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Comparisons of the ecology and stable isotopic compositions of living (stained) benthic foraminifera from the Sulu and South China Seas
Pergamon PII:
Deep-Sea Research I, Vol. 43, No. 10, pp. 1617-1646,1996 Copyright Q 19% Elsevicr S.zieaceLtd Printed inGreatBritain. AU rights mened S0967-0637@6)00071-4 0967-0637/96$15.00+0.00
Comparisons of the ecology and stable isotopic compositions of living (stained) benthic foraminifera from the Sulu and South China Seas A. E. RATHBURN,*$ B. H. CORLISS,* and K. C. LOHMANNt
K. D. TAPPA*
(Received 28 April 1995; in revisedform 20 March 1996; accepted 26 April 1996)
Ah&act--Significant differences are observed between living (Rose Bengal stained) deep-sea benthic foraminifera found in 14 box cores (510-4515 m) from the thermospheric (> 10°C) environments of the Sulu Sea and the psychrospheric (< 10°C) conditions in the South China Sea. Gavelinopsis, Bolivinopsis, Astrononion, Osangularia and Ceratobulimina are common taxa in the South China Sea, but are rare to absent in the Sulu Sea; Siphonina and Valvulineria are dominant genera at certain depths in the Sulu Sea, but are rare to absent in the South China Sea. Fauna1 differences appear to result from large differences of the bottom-water temperatures (differences from about 6 to 8’C) between these basins. Fauna1 abundance patterns within each basin are suggested to be related to the organic carbon contents in the sediments, since temperatures, salinities and dissolved oxygen levels of the bottom-waters are relatively uniform. The 8’*0 values show a > 2%~range and are similar to those presented by previous workers, but have no consistent relationship with microhabitat preferences. Vertical distribution patterns and carbon isotope compositions of species, however, reflect microhabitat preferences and are consistent with previous observations from other regions. Epifaunal species (O-l cm interval) such as Cibiciakndes pachyderma, Ctbictdoiaks wuellerstorf, Hoeglundina elegans and Anomalinoides colligera, have higher 813Cvalues than taxa which have the ability to live deeper within the sediments. Infaunal taxa that live in the upper 2-3 cm, including Uvigerina peregrina, Uvigerina proboscidea, and Bulimina mexicana, have lower 6°C values than epifaunal species, and the deep infaunal species, Chilostomelia oolina, has the lowest 6% Cibicidoides bradyi and Oridorsahs umbonatus are found between 0 and N 4 cm and have lower carbon isotope values (by > 1.4!%0in some cores) than epifaunal Cibicidoides species. Exceptions to this pattern include the aragonitic species, Gavelinopsb lobatulus, (0-4cm) which produces significantly lower 813C values than deep infaunal taxa, and the shallow infaunal species, Ceratobulimina paczfica (also aragonitic) and Bolivinopsis cubensis (deep infaunal), which yield higher carbon isotopic values than epifaunal taxa. These exceptions are found primarily in only one core, and additional samples are needed to confirm the relationship between their distribution patterns and isotopic compositions. Each of the species examined has a relatively consistent 813C value throughout its distribution within the sediments that may result from heterogeneity of microhabitats within the intervals sampled. Intrageneric differences in 8% of Cibicidoiaks, and possibly Uvigerina and Bulimina, are evident. The isotopic differences between C. bradyi and many other Cibicidoides species are related to differences in microhabitat preferences between species. The 8i3C results confirm the influence of microhabitat preferences on the carbon isotopic composition of deep-sea benthic foraminifera and reaffirm the importance of assessing the microhabitat preferences of species used for isotopic analyses. Copyright 0 1996 Elsevier Science Ltd
*Department of Geology, Duke University, Durham, NC 27708, U.S.A. 7 Department of Geological Sciences, University of Michigan, Ann Arbor, MI 48109-1063, U.S.A. $Present address: Scripps Institution of Oceanography, Marine Life Research Group, 9500 Gihnan Drive, La Jolla, CA 92093-0218, U.S.A. 1617
1618
A. E. Rathbum et al.
Fig. 1. Regional map of the study area with Western Caroline Basin cores plotted and bathymetric map of the Sulu and South China Seas inset area showing box core locations. Depth contours in meters.
INTRODUCTION Distribution patterns of deep-sea benthic foraminifera and the stable isotopic compositions of their tests have been extremely useful as indicators of paleoceanographic conditions. In order to accurately infer ancient bottom-water conditions from fossil benthic foraminifera, we must understand the factors which influence the distribution of benthic foraminifera and determine the relationships between foraminiferal shell chemistry and environmental and ecological parameters. The uniform bottom-waters of the Sulu Sea and the contrasting bottom-water properties of the adjacent South China Sea furnish a natural setting for a comparative study of the ecology of benthic foraminifera and the geochemistry of their shell material. Observations on the ecology and isotopic composition of species living in these basins can be applied to the interpretation of fossil assemblages from a variety of settings in the world ocean. This paper focuses on (i) comparisons of fauna1 distribution patterns in the warm ( > 1O’C) Sulu Sea with those found in the cooler South China Sea; and (ii) the relationships between benthic foraminiferal stable isotope compositions and microhabitat preferences.
STUDY
AREA
Sulu Sea
Located between the Philippine Islands and Sabah (Borneo), the Sulu Sea is an isolated marginal basin (250,000 km2), surrounded by sills which are generally less than 200 m deep (Exon et al., 1981) (Fig. 1). South China Sea intermediate water flows through a single 420 m deep channel in the Mindoro Strait, providing the only source of deep water to the Sulu Sea basin (Van Riel, 1943; Wyrtki, 1961; Frische and Quadfasel, 1990). As a result, the Sulu Sea is a thermospheric (> 1O’C) basin with uniform salinities (- 34.5), warm temperatures (- lO.S”C), and low dissolved oxygen values (- 55 pM x 1.25 ml 1-l) in water depths below
1619
Ecology and isotopic composition of foraminifera SOUTH CHINA SEA (4
(b)
‘J
TEJWRRATURE
(‘Cl
SUL.U SEA
_ -11
SOUTH CHINA SEA
DISSOLVED OXVGRN (mL’L)
SULAJ SEA
*.,s -
Fig. 2. Schematic drawing showing: (a) temperature distribution in the South China Sea and Sulu Sea; surlicial organic carbon, schematic core depth distribution and dominant genera (> 10% of calcareous assemblage) for the > 150 pm and > 63 pm fractions are also plotted. Parentheses refer to taxa which comprise > 10% of the calcareous assemblage in one subcore, but not in the duplicate subcore; (b) oxygen distribution in the South China and Sulu Seas.
1000 m (Fig. 2 and Table 1). The aragonite compensation depth is at 1400 m, and the calcite compensation depth occurs at 4500-4800 m (Exon et al., 1981; Linsley et al., 1985). Surfkial sediment organic carbon contents ranged from > 0.10% to > 2.5%; the highest values
1620
A. E. Rathburn er al.
Table 1. Core locations, water depth (m), number of taxa, standing stocksfor > 150 pm and > 63 pmfractions (no. per 50 cm2), bottom-water oxygen levels (@I), temperatures (“C), salinities (V&I), calculated 6”O of equilibrium calcite (S’80,,,(~PDB)), and calculated 6’3C of the ambient bottom-water (613Cb.,,(%PDB)) (see text for discussion)
Standing stock (No. per 50 cm2) > 150pm >63pm CO=
Depth
Sulu Sea 12 510 8
1005
Lat. (‘NJ
Long.
(“E)
Total
TOtal
TOtal
Total
No.
01
Temp.
foram.
talc.
foram.
CA.
SPP.
(PM)
(“C)
2416
1237
II2
8” oz.!?
118” 22.4
1305
437
8” 08.5
118” 35.0
2982
1063 II58
Sal. %n
6’80 cc.
S’=O b.w.
K
?fa
78.5
11.06
34.46
1.38
73
71.8
10.10
34.45
1.61
-0.03
0.06
10
1980
8” 20.6’
118” 57.6
605
84
322
49
57.2
IO.15
34.46
1.60
-0.15
9
1995
8” 20.6
118” 57.9
612
137
964
278
39
55.9
IO.15
34.46
I.60
-0.15
20
3000
6” 54.5
119” 10.0
557
44
937
110
32
53.8
10.29
34.41
1.56
-0.15
15
3995
7” 33.9
120” 19.8
66
II
88
I3
IO
54.6
10.46
34.47
I6
4000
7” 32.9
120” 19.5
472
21
145
55
13
53.8
10.46
34.47
18
4515
7” 25.3
121” 12.5
110
I75
199
I4
53.6
10.54
34.47
2046
639
44
89.1
4.19
3.11
- 0.20
316
59
20
103.2
2.48
109.3
3.56
-0.16
II9
South China Sea 3
1095
10” 57.3
118” 27.5
4
2150
I I” 53.3’
llE”20.4
2
2950
12” 07.1’
118” 03.6
162
7
6
I
3980
13” 36.5
117O41.2
584
70
6
2.45 2.46
Western Caroline Basin 23
3025
7” 37.1’
138” 47.7
84
I9
22
3515
7” 18.6
138” 11.0
40
I6
165
86
19
146.4
1.60
34.67
I5
156.9
1.50
34.68
occurred between 500 and 1200 m, and the lowest values were found on the western shelf and in the central basin. Organic carbon values > 1% were found in turbidites below a depth of 4500 m (Exon et al., 1981). South China Sea Located immediately west of the Sulu Sea, the South China Sea is also a semi-enclosed basin with maximum depths exceeding 5000m (Fig. 1). Bottom-waters are derived from intermediate and deep waters of the Pacific Ocean which flow through the 1900 m deep Bashi Channel in the Luzon Strait (Broecker et al., 1986), located between Taiwan and Luzon (Van Riel, 1943; Wyrtki, 1961). As a result, South China Sea bottom-waters have psychrospheric temperatures of approximately 2.4”C and oxygen levels of over 1.75 ml 1-l x89 uM in the deeper portions of the basin (Fig. 2, Table 1). The aragonite compensation depth of the South China Sea is between 1000 and 1400 m, and the calcite compensation depth is about 38004000 m (Rottman, 1979; Thunell et al., 1992). In the South China Sea area examined in this study, productivity is probably similar to that of the study area in the Sulu Sea. In the study area north of Palawan in the South China Sea, Thunell et al. (1992) and Kuehl et al. (1993) noted that there is no evidence of significant variations in productivity and assumed uniform productivity for the sector. Possible differences in primary productivity of the area are evidenced by higher levels of barite in the sediments of this sector compared with the southeastern South China Sea and the Sulu Sea (Calvert et al., 1993), but organic carbon accumulation data suggest that this is not the case. Organic carbon contents of the sediments increase slightly with depth in this portion of the South China Sea, but there is no evidence of upwelling in this area (Thunell et al., 1992;
Ecology and isotopic composition of foraminifera
1621
Calvert et al., 1993). Upwelling in the Sulu Sea is unlikely due to the hydrography of the basin and the geographic positioning with respect to the prevailing winds (Wyrtki, 1961). As a result, the South China Sea sector examined in this study and the Sulu Sea are thought to have similar primary productivity values ranging from 60 to 100 gC mm2 year (Berger, 1989; Thunell et al., 1992; Kuehl et al., 1993). PREVIOUS
WORK
Benthic foraminiferal distributions
Recent studies of modern benthic foraminifera in the Sulu Sea have noted that the distribution of assemblages is variable within the basin (Exon et al., 1981; Linsley et al., 1985; Rathburn and Corliss, 1994). Based on > 150 pm fraction data from four piston cores and nine surface sediment samples, Linsley et al. (1985) suggested that the faunas are controlled primarily by bottom-water oxygen levels and the quantity of organic carbon. From samples also included in this study, Rathburn and Corliss (1994) demonstrated that living (Rose Bengal stained) assemblages from eight box cores vary with depth, despite the uniformity of bottom-water properties. Rathburn and Corliss (1994) concluded that the oxygen content in the bottom-water does not control fauna1 distributions, including taxa previously characterized as indicators of low oxygen conditions, and suggested that the benthic faunas are influenced by the organic carbon content of the sediments. The influences of bottom-water oxygen concentrations and organic carbon on benthic fauna will be considered in detail later in this paper. The relatively few studies that have focused on recent benthic foraminifera in the South China Sea include those of Polski (1959) in the East China and Yellow Seas, Biswas (1976) on the Sunda Shelf, and Waller (1960) along the western margin of the South China Sea. Miao and Thunell(1993, 1995) examined benthic foraminifera from gravity cores taken in the Sulu and South China Seas and concluded that organic carbon and oxygen penetration depth affect the distribution of benthic foraminifera in both basins. Stable isotope studies
Intraspecific and interspecific differences in stable isotopic compositions of benthic foraminifera have been documented by a number of researchers, and both positive and negative correlations between 6i3C and al80 have been reported (e.g. Duplessy et al., 1970; Woodruffet al., 1980; Belanger et al., 1981; Graham et al., 1981; Grossman, 1984a,b, 1987; Mackensen and Douglas, 1989; McCorkle et al., 1990). Isotopic differences between benthic foraminifera species have been attributed to various factors, including the incorporation of metabolic products into the test, ontogenetic differences and other “vital effects” (biological differences which result in differences in isotope fractionation), as well as environmental and microhabitat effects (Grossman, 1984a,b, 1987). By comparing glacial and interglacial carbon isotopic values, Zahn et al. (1986) suggested that the 613C values of the infaunal “Uvigerina peregrina group” correlated with organic carbon accumulation rates, and carbon isotope values of the epifaunal species, Cibicidoides wuellerstor-, were related to bottom-water isotopic composition. McCorkle et al. (1990) found that 13Ccompositions of epifaunal taxa are related to the isotope values of bottom-waters and that specimens with deeper microhabitat preferences yield lower isotopic signals more closely correlated with
1622
A. E. Rathbum et al.
pore-water isotope values. This correspondence between microhabitat preference and isotopic composition indicates that the carbon isotopic values of benthic foraminifera are at least indirectly influenced by ecological preferences. Interspecific differences between taxa found in the same interval within the cores were also noted, however, indicating that vital effects do exist for some species. METHODS This investigation is based on the analysis of deep-sea benthic foraminifera from 14 Soutar box cores taken on depth transects from 510 m to 4515 m in the Sulu Sea (eight box cores), 1095-3995 m in the South China Sea (four box cores) and two cores (3025 m and 3515 m) from the Western Caroline Basin (Fig. 1, Table 1) collected on the R.V. Moana Wave in August 1988. Subcores (10.1 cm interior diameter clear plastic tubes) were taken from each of these box cores and subsampled in 0.5 cm intervals down to 3 cm, and 1 cm intervals down to 20 cm; each sample was preserved in 4% formalin bu.Bered with Mule Team Borax. For a complete description of the procedures, see Rathburn and Corliss (1994). Oxygen levels, salinities and temperatures in the water column were measured with a Sea Bird profiling CTD equipped with a dissolved oxygen sensor and attached to the box corer, and bottom-waters sampled with Niskin bottles attached to the box corer were also analyzed for oxygen content by Winkler titrations. A minielectrode (Helder and Bakker, 1985) was used to measure the oxygen levels of the porewaters in the sediments of one subcore from each box core except core 1, in which porewater manganese measurements indicate the level of pore-water oxygen penetration (see Rutgers van der Loeff, 1990). Organic carbon weight percentage measurements were made with a Carlo Erba NA 1500 Carbon-Nitrogen-Sulfur Analyzer following the procedure outlined by Lu and Emerson (1987), which is based on methods established by Froelich (1980). In the laboratory, 65 ml Rose Bengal stain solution (1 g 1-i of 4% formalin) was added to each subsample and allowed to stain for at least one week before processing. The sample was then wet sieved using 63 pm and 150 pm sieves. Only the results of the > 150 pm fraction are discussed in this paper. Some Sulu Sea samples were wet-split with a modified Folsom plankton splitter because of the large volume of material in each sample (up to N 100 ml). Each sample was placed in a gridded petri dish with water, and Rose Bengal stained benthic foraminifera were picked from the sample, placed on a micropaleontological slide, identified, and counted. Sulu Sea fauna1 data are based on the analysis of one subcore per box core, whereas South China Sea data are based on two subcores per box core. Species with sufficient specimens for isotopic analyses from subcores 12-2, 8-1, 10-2, 16-2,18-2 in the Sulu Sea and l-2 and 3-2 in the South China Sea were analyzed for carbon and oxygen isotopes at the University of Michigan. All samples were roasted at 380°C and reacted at 73°C with four drops of anhydrous phosphoric acid in a Finnigan MAT carbonate extraction system (“Kiel device”) connected directly to a Finnigan MAT 251 isotope ratio mass spectrometer. Data are reported in the standard 6 notation relative to the Peedee Belemnite (PDB) standard. Precision and calibration of the data were checked with NBS-20 powdered carbonate, and analytical precision was better than 0.1% for both carbon and oxygen isotope analyses. The small volumes of material used for some samples in this study produced variability (standard deviation of > 0.05) in the stable isotope signal detected by the mass spectrometer; these values are marked with parentheses in Table 3 and are not used in the analyses.
Ecology and isotopic composition of foraminifera Table 2.
1623
Microhabitat preferences for selected Sulu Sea and South China Sea taxa
Microhabitat preferences Transitional (O-4 cm)
Epifauna (O-l cm)
Cibicidoides bradyi Cibicidoides robertsonianus Gavelinopsts lobatulus Melonis ajfinis Osangularia culter Oridorsalis umbonatus Siphonina reticulata
Anomalinoides colligera Cibicidoides pachyderma Cibicidoides wuellerstorfi Hoeglundina elegans
Deep infauna ( > 4 cm)
Shallow infauna (&2 cm)
Bolivinopsis cubensis Chilostomella oolina Valvulineria mexicana
Ammonia beccarii Astrononion novozealandicum Bulimina marginata Bulimina mexicana Ceratobuliminapactj?ca Globocassidulina subglobosa Gyroidinoides broeckhiana Pullenia bulloides Trifarina bradyi
Vvigerinaperegrina
RESULTS Vertical distribution patterns of individual taxa, pore-water oxygen content, sedimentary organic carbon, and stable isotope compositions of abundant calcareous taxa are summarized in this section. Fauna1 data (No. per 50 cm3) for the Sulu Sea are given in Rathburn and Corliss (1994), and fauna1 data for South China Sea cores are included in Tappa (1992). Standing stock data from two box cores taken in the Western Caroline Basin are presented in Table 1. Lists of the dominant genera ( > 10% of the calcareous fraction) in the > 150 urn fraction for each core are shown in Fig. 2. Pore-water oxygen data are taken from Rutgers van der Loeff (1990) and unpublished data and information on mixing coefficients and sedimentation rates are from Fuglseth (1991) and Kuehl ef al. (1993). Microhabitat designations are given in Table 2, and carbon and oxygen isotope results are given in Table 3.
South China Sea fauna The > 150 urn fraction of two subcores from each South China Sea box core were examined to assess heterogeneity within a box core. Fauna1 data are plotted with a line connecting the averages of the two subcores at each depth interval (vertical bars represent fauna1 densities from each of the subcores) (Figs 3-6). Differences in abundances of taxa may exist between subcores taken from the same box core, but fauna1 patterns are similar. The microhabitat preferences of dominant fauna are given in Table 2, and fauna1 data from each core is presented in detail in Rathburn (1992); only a few brief comments are included below.
1624
A. E. Rathburn et al.
Table 3. Stable isotopic values (?60 relative PDB) for Sulu Sea and South China Sea taxa. Sample which generated variable isotope signals (standarddeviation of > 0.05) are denoted withparentheses. The number of specimens usedfor each analysis are also included
Sulu Sea Interval
core
Species
613C
South China Sea 6’*0
Number of Specimens
Interval
Species
613C
S’*O
Number of Specimens
12
o-1
A. co&era
-0.17
0.56
5
O-l
A. novozeahmdicum
-0.59
0.52
7
34
B. cubemis
(0.91)
O-l
B. marginolo
-0.58
I .26
7
4-5
B. cubenris
0.87
(1.5) 1.41
22
CL1
B. mexicana
-1.08
1.31
11
5-6
B. cuben&
0.78
1.12
11
&I
C. bradyi
(-0.38)
(1.3)
5
t-7
B. cubenris
0.94
1.31
18
l-l.5
C. bradyi
-0.37
1.06
2
7-8
B. cubensis
0.81
I .22
8
c-l
C. pachydenna
(1.21)
(3.05)
3
a9
8. cubenris
(0.39)
(0.79)
9
I-l.5
C. pochydenna
0.39
0.8
2
9-10
E. c!hnsis
(0.36)
(0.47)
5
34
C. pachyderma
0.38
1.01
2
l&11
8. cubensis
0.92
1.45
9
(0.29)
(I) (1.74)
6
11-12
B. cubenris
0.8
1.29
8
6
1314
B. rubensir
(1.03)
(1.48)
10 7
O-l
c. wut?llerstorji
&I
H. errgaIL
1.55
Core 3 6
l-l.5
H. &gals
1.4
1.78
2
14-15
8. cubensis
0.73
1.13
67
H. ekgans
1.64
1.67
I
I.%16
B. cubensis
0.99
1.28
5
C-l
M. a/fvris
-0.42
0.69
6
16-17
B. cubensis
0.95
1.3
IO
o-l
0. umbonorw
-0.92
1.26
2
17-18
B. cubensis
0.82
1.3
8
1.s2
P. bulioides
-1.3
1.44
4
19-20
B. cubensis
0.9
I .43
13
o-l
S. reticulafa
-0.41
1.02
7
0.51
c. pact@ica
1.46
3.31
7
c-l
CJ. proboscidea
-0.44
1.28
II
1.5-2
c. pqgica
1.3
3.26
2
(-0.58)
(1.38)
3
v. peregrina
O-l core
8
1 l-12
c. pacififo
I .48
3.26
5
67
c. oolina
-1.81
3.06
35 20
45
A. beccarii
-0.11
1.41
2
7-8
c. oolino
(-1.93)
(3.27)
13-14
A. beccorii
(-0.14)
(1.47)
1
O-o.5
C. bradyi
-0.64
2.39
4
&I
A. eolligera
-0.02
0.72
I
0.5-I
C. bradyi
(-0.56)
(2.48)
8
l-l.5
A. co&era
0.11
0.66
1
l-l.5
C. bradyi
-0.59
2.6
2
4-5
A. col@era
0.15
0.78
2
Is-2
C. bradyi
-0.72
2.55
7
&I
B. mexicana
-0.67
1.52
2
O-O.5
Cibicidoides
spp.
-0.01
2.3
3
2-2.5
C. oolino
(-3)
(-0.03)
4
0.5-l
Cibicidoides
spp.
-0.13
2.28
3
7-8
C. oolina
(-2.36)
4
(MS
G. lobaruhu
-3.57
1.61
8
2-2.5
C. pachyderma
(0.28)
(0.2) (0.94)
2
0.5-I
G. lobattdur
-3.42
1.56
6
2.>3
C. pachyderma
I .08
2.18
2
2-2.5
G. lobandw
(-2.69)
(1.67)
2
1314
C. pachyderma
0.34
0.91
3
15-16
G. lobandw
(-3.36)
2
&I
M. affmis
(-0.57)
(1.13)
2
3-l
G. svbxlobosa
(-0.54)
(I .w (2.76)
8-9
h4. aJjjmic
-0.13
0.98
2
12-13
G. subxlobosa
-0.71
2.91
3
O-l
S. rericulara
-1.09
-0.71
4
GO.5
0. c&v
-0.55
2.81
9
2-2.5
S. reticulum
-0.07
1.09
2
SO.5
u. peregrina
-0.72
2.85
4 3
I
2.5-3
S. reticulara
-0.03
1.2
2
0.5-I
u. peregrina
-0.79
2.76
4-5
S. reficulafa
(-0.06)
(1.15)
2
l-l.5
[I. peregrina
(-0.88)
(2.69)
I
5-6
s. rericldara
-0.1
I.15
3
0.5-I
U proboscidea
(-0.58)
(2.71)
3
7-8
S. reticulara
-0.01
1.23
2
3-4
U. proboscidco
-0.34
2.77
5
9-10
s. retic!&ta
(0.35)
(1.67)
2
67
U. proboscidea
-0.41
2.52
6
12-13
S. reticulatrr
-0.1
1.09
2
Core 1
13-14
s. retic!Jara
10
1314 O-1
T. bradyi
(1.36)
2
7-a
c. oolina
-2.39
3.44
(1.93) 1.55
2 2
8-9 %I0
c. oolina
-2.33
3.46
0. umbonarus
(-0.89) -1.12
c. oolino
-2.62
3.49
5
6-7
0. umbonatur
-0.75
1.29
I
10-11
c. oolina
-2.55
3.46
9
12-13
1.46
2
11-12
C. oolina
(0.28)
5
0. umbonlrrur
-0.68
-2.32
3.51
10
O-1
U. proboscideo
-0.28
1.43
4
12-13
c. oolina
-2.47
3.45
8
l-l.5
lJ. probaxidea
2
13-14
C. oolina
-2.42
3.5
9
I.>2
U. proboscidea
(0.06) -0.27
(1.82) 1.37
2
2%3
v. proboscidea
-0.32
1.16
2
8-9
U. proboscidea
-0.28
1.11
3
e10
U. proboscidea
-0.18
1.16
2
11-12
U. proboscidea
(-0.2)
(1.93)
3
1314
u. probosc&&a
-0.33
1.37
5
14-15
U. proboscideo
-0.15
1.33
4
IS16
U. proboscidea
-0.26
1.44
2
(continued)
1625
Ecology and isotopic composition of foraminifera Table 3. sllhl Interval
Species
Continued
sea 613C
South China Sea #*O
Numberof
Interval
Specimens
613C
g’s0
Number of
Specimens
10
Con O-1
C. bradyi
(-0.08)
(1.22)
5
l-l .5
C. bradyi
-0.32
1.11
4
1.5-Z
C. bradyi
-0.14
I .24
3
2-2.5
C. bradyi
-0.04
1.23
3
o-1
c. wwllers10rfi
0.19
0.96
3
O-l
G. broeckhiaw
-1.09
I .46
2
&I
0. umbonorru
-1.28
1.4
4
0. umbonarus
-1.19
1.39
4
(-0.03)
(1.1)
3
-0.76
1.13
2
1.5-2 core
Species
20
O-l
C. bradyi
O-1
C. robertsonionur
0-I
0. !mlbomzur
(-0.59)
(1.44)
2
I .5-z
0. umbonorw
-0.65
1.31
2
3.5-4.5
0. umbonatw
-0.77
I .32
3
0. umbonatur
(-1.4)
(I .53)
3
2-2.5
V. mexicana
(-0.72)
(1.1)
17
2.5-3
V. mexicana
(-0.76)
(1.12)
22
Core 16 &I core
18
South China Sea Core 3 (1095 m) >150 pm (#/Socc) Clblddddfs bradyi
Ceratobnhntnn pdfka
Fig. 3. Vertical profiles of selected species from the > 150 pm fraction of core 3 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 data from subcores 3-1 and 3-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
1626
A. E. Rathbum et al.
South China Sea Core 4 (2150 m) ~450 pm (W&c) OrbbmaUs umbmatua 0 0
5
10
paclfka
centobulbnbu
15
r-0
Organic
0.0
03
15
10
I
Carbon
0.4
0.6
4.
0.8
Fig. 4. Vertical profiles of selected species from the > 150 pm fraction of core 4 (no. per 50 cm’) plotted vs sediment depth (cm). Fauna1 data from subcores 4-l and 4-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
Agglutinated foraminifera dominate the > 150 pm fraction of the South China Sea subcores and reach maximum densities in the top 1 cm in subcores from the 1095 m site (core 3) in one subcore from the 2150 m site (subcore 4-l), and in one subcore from 2950 m (core 2-l). The remainder of the subcores examined show density maxima of the agglutinate assemblages below the upper 1 cm. Graphs and data tables of total agglutinated assemblages are included elsewhere (Tappa, 1992). The presence of relatively large numbers of stained specimens deep in the sediments in core 3 is similar to patterns seen from water depths of 1200 m or less in other regions (Loubere and Gary, 1990; Corliss and van Weering, 1993). Since micro-scale gradients in oxygen (Meyers et al., 1987, 1988; Langer et al., 1989; Thomsen and Altenbach, 1993) and increases in organic carbon contents near macrofaunal burrows (Aller and Aller, 1986) have been shown to influence meiofaunal abundances and distributions, subsurface fauna1 patterns in core 3 are interpreted to result from suitable deep infaunal habitats created by macrofaunal burrowing. Laboratory X-radiographs showed evidence for extensive bioturbation throughout the length of core 3 sediments. Fauna1 abundances of the > 150 urn fraction in core 2 are relatively low, and based on a qualitative examination of the 63-l 50 l,trn fraction of surficial sediments of this core, the smaller size fraction also does not contain high fauna1 abundances. In contrast to the relatively diverse assemblage in core 3 (1095m), core 1 (3980m) is characterized by a low-diversity, infaunal assemblage dominated by Chilostomella oolina. The absence of a stained epifaunal assemblage, combined with the presence of abundant, living infauna in core 1, indicate that this assemblage represents a living population, and does not result from enhanced preservation due to rapid burial. The increase in C. oolina
1627
Ecology and isotopic composition of foraminifera
south china sea Core 2 (2950 m) >150 pm (#/gocc)
Of
01
0.4
0s
0.6
0
30
so
90
no
0
5
$
1
F
15
IO
~
Fig. 5. Vertical profiles of total calcareous taxa and total foraminifera from the > 150 pm fraction of core 2 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 dam from subcores 2-1 and 2-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
South China Sea Core 1 (39gom) >150 pm (#lsocc)
0-k
Cubm
%
Fig. 6. Vertical profiles of total calcareous taxa and total foraminifera from the > 150 urn fraction of core 1 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 data from subcores l-l and l-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
1628
A. E. Rathbumet al.
densities at 6-8 cm in this core coincides with an increase in agglutinate densities (which also have an infaunal density maximum) and a sharp increase in organic carbon contents (Fig. 6). The X-radiograph of the reference subcore shows evidence for bioturbation throughout the core, with no observable turbidite features. The significant increase in subsurface organic carbon contents, together with unusually high organic carbon contents at this water depth, however, are consistent with the occurrence of turbiditic sedimentation. Calvert et al. (1993) note that 8t3C,rsanic values of the surficial sediments of both the Sulu and South China Sea basins do not decrease uniformly with increasing water depth, suggesting that there is organic matter input from shallow-water or terrestrial sources to deep water environments. There is no hydrological evidence for a localized region of high productivity in this area of the South China Sea, and the relatively high organic carbon values probably result from the transport of organic-rich sediments from shallower depths via turbidites; bioturbation has obscured many of the laminations characteristic of turbidites. Pore-water oxygen levels were not measured in this box core, but the pore-water Mn profile suggests that pore-water oxygen values reach zero between 8 cm and 10 cm (Fig. 6). Box core 1 has the highest apparent mixing coefficient of the box cores examined by Fuglseth (1991), at about 1.5 cm* year- ‘. Sulu Sea fauna
Detailed fauna1 and geochemical results of Sulu Sea cores are given in Rathbum and Corliss (1994), and microhabitat preferences of dominant taxa are given in Table 2. Vertical distribution patterns of abundant species used in isotope analyses are shown in Figs 7-10. Fauna1 data from other cores are presented but are not illustrated. Oxic pore-water penetration depths and surficial organic carbon values for Sulu Sea cores are plotted in Fig. Il. Only a few brief comments regarding cores 8 (1005 m) and 18 (45 15 m) are given below. Rathburn and Corliss (1994) attributed the occurrence of relatively large densities of stained benthic foraminfera at 13-16 cm in core 8 (1005 m) to a rapid burial event which preserved an epifaunal assemblage by preventing significant degradation of protoplasm. Recolonization of the surficial sediments and preservation of the buried organic material (including protoplasm) would produce the observed fauna1 patterns (Fig. 8). The occurrence of a rapid burial event is also supported by laboratory X-radiographs, sedimentation rates and subsurface organic carbon patterns (Rathburn and Corliss, 1994). Although turbidite sedimentation is evident in core 18 (4515), Rathbum and Corliss (1994) have noted that the fauna1 patterns are not consistent with a rapidly buried assemblage, but instead indicate that stained specimens represent the living population (Fig. 10). The calcareous assemblage of core 18 (4515 m) consists of over 14 species found primarily below 1.5 cm. The > 150 urn and > 63 urn fractions are dominated by Vulvulineriu mexicana, which has a maximum in the 2.5-3 cm interval (Fig. 10). Maximum abundances of Globobulimina sp. 2 are found between 8 and 10 cm, while specimens of Chilostomella occur between 5 and 11 cm. Organic carbon contents are significantly higher in core 18 compared to values obtained from the 3000 and 4000 m cores (Figs 10 and 11) and show a significant maximum (-0.9-l .5%) at 8-l 1 cm (Fig. 10). Onboard X-radiograph analysis and 14C profile data indicate that turbidite sedimentation influenced box core 18. The relatively high organic carbon values at this depth coupled with the sharp subsurface maxima in organic carbon are also consistent with the suggestion that turbiditic sedimentation occurred.
1629
Ecology and isotopic composition of foraminifera
Sulu Sea Core 12(510m) >150pl (#/5occ) Clbkldddes 0
pacby&rms LO
5
Bollmloa IS
Uvigerbw
mukans
5
to
I5
0
pcregrlna
s
LO
15
*I+-Clbkldolda
0
5
nvelkrstwfl
to
15
20
I
Fig. 7. Vertical profiles of selected species from subcore 12-2 (no. per 50 cn?; > 150 pm fraction) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with symbols in Fig. 12.
Sulu Sea Core 8 (1005 m) >150 pm (#/SOcc) Anomallnddar 0
5
Clbkldokka
cdll~en
16
IS
Uvlgerlna 20
pachyderma
0
to
SIphonIns
0rldorpslls
pmbosdda 20
rrtkulnta
30
0
5
umbonatus 10
Melonis
IS
Chllostomelk 20
0
s
10
oollns IS
Pmnls
Fig. 8. Vertical profiles of selected species from subcore 8-l (no. per 5Ocm’; > 150 urn fraction) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with symbols in Fig. 13. Hatched areas mark buried top interval.
20
1630
A. E. Rathbum et al.
Sulu Sea
Core 10W80
m)
>lSO pm W*C)
(a) Clbkldoldeo dkrstdl
Clblddotdes
Gymtdlnotda
bradyi
brocdtbtana
L-2 , 0
10
Sulu Sea Core 2OW@m) >lSO pm WOcc)
(b) Ctbtctdddrr 0
5
Ortdor~alts umlmaatus
bradyl to
Clbkldoidrs
0
15
mberkonlsnus 5
10
IS
Fig. 9. (a) Vertical profiles of selected species from the > 150 pm fraction of subcore 10-2 (no. per 50cm3) plotted vs sediment depth (cm). (b) Vertical profiles of selected taxa from the > 150 urn fraction of subcore 20-2 (no. per 50cm3) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with
Sulu Sea Core 18 4515 m (#/xkc) >150 pm
Fig. 10. Vertical profiles of selected species (no. per 50 cm’) from the > 150 )rm fractions of subcore 18-2 plotted vs sediment depth (cm); organic carbon and pore-water oxygen contents are also plotted.
Ecology and isotopic composition of foraminifera Pore-Water Oxygen Penetration Depth (cm) 10
5
0
0
15
1631
Surfidal Organic Carbon 96 20
ib
0.4 0.5 0.6 0.7 0.8 0.9 1.0
1000
F
Fig. 11. Oxic pore-water penetration depth (cm) and surficial organic carbon (weight %) for each Sulu Sea core plotted vs sediment depth (cm).
Sulu Sea stable isotope analyses
The 613C and 6r80 values of abundant taxa are given in Table 3. Samples which yielded isotope values with a standard deviation of > 0.05 are shown in parentheses and are not included in the figure plots or discussed in the text. The isotopic composition of specimens from cores 15, 16, and 18 were not determined because of low numbers of specimens, and core 9 specimens were not analyzed for isotopes because core 9 was taken at the same site as core 10. Analyses of X-ray diffraction data showed that Bolivinopsis cubensis has a calcitic test, while the test of Gavelinopsis lobatulus is aragonitic. The other aragonitic taxa included in the isotope analyses are Ceratobulimina pacljica and H. elegans. The distribution of carbon and oxygen isotope data for each taxon in Sulu Sea cores is presented in Figs 12 and 13, while Fig. 14 illustrates the distribution of stable isotope data from core 3 (1095 m) in the South China Sea. The average oxygen isotope differences (A6180) between test 6180 and the calculated at80 of equilibrium calcite (8’80,.c.), and the average carbon isotope differences (A613C) between estimated bottom-water 613C (6’3Ct,,.) and test 613C for each taxon with more than one isotope analysis are presented in Fig. 15. For the purpose of comparison, the 8180 (PDB) of calcite in equilibrium with water (6180,,c,, PDBj) of a given 6180 SMOW composition (8’80((b. w,. SMOW))and temperature T (in degrees Kelvin) was calculated using the following equations (provided by D. McCorkle, personal communication, 1995): J’80+.,~~~~
=
Ie
x ~180 ((2.78xlo'/T2)-(2.89/10')) (b.w.,SMOW) + 1000)) - 1000
6180(,,.,poaj = (0.97006 x S’80~,.,.,s~ow$ - 29.94
(1)
(2)
Equation (1) is based on the temperature relationship given in equation (3) from Friedman and O’Neil(1977), and differs slightly from the equations given in McCorkle et al. (1990) that are based on equations from O’Neil et al. (1969). 10’ln cr(CaCOs - H20) = 2.78 x lo/T2 - 2.89.
(3)
We estimated bottom-water 8180 (6’80t,w.) to be - 0.1% SMOW for each site (based on western Pacific Water intermediate- and deep-water values). Without bottom- or surficial pore-water 613C data, it is difficult to accurately estimate the 6r3C of equilibrium calcite (Sr3C,.,.) in the Sulu and South China Seas. Northern Pacific
A. E. Rathbum et al.
1632
Sulu
sea PO (4&d
613C (%I
Core 12 (510 m)
~
,jyk$y
B
y&L
j-
j_L+z
Core 10 (1980 m)
m Astmnonbn novomahdknm
~~~~~~~
~~~~
~~~~~n~l ?? CibWdcddeabndyl
Fig. 12. The gL3Cand 6rsO values (%o)for significant species from subcores 12-2, 10-2, and 20-2 are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (6) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each species are also indicated. Because of the number of data points, the data have been separated into four plots.
Ocean GEOSECS stations 222,224,226,229,235,241,246, and 251 include bottom-water F13Cvalues from appropriate depths (near 400 m, for Sulu Sea estimates, and 1000 m down to N 2000 m for South China Sea estimates), but even using the correction factors suggested by Kroopnick (1985), the data are variable. As noted by McCorkle and Keigwin (1994), GEOSECS 613C data from many of the western Pacific sites are equivocal, especially those from the upper 1000 m of the water column, making it difficult to assess the 613Ccomposition of water moving into the South China and Sulu Sea Basins. For this reason, we have chosen to estimate the 6r3C value of bottom waters in the Sulu and South China Seas based on the relationship between apparent oxygen utilization (AOU) and 613C given in Kroopnick (1985). Using the relationship between AOU (AOU = (dissolved oxygen at saturation) (measured dissolved oxygen levels)) and 613C as presented in Kroopnick (1985) (equation (4)) and the solubility of oxygen at measured temperatures and salinities given in Weiss (1970), 613C values were calculated for bottom-waters in the South China and Sulu Seas. 613C = 1.5 - 0.0075 x AOU
(4)
Ecology and isotopic composition of foraminifera
Sulu
8
sea
Core (1005 m)
(%cPDW PO
Fig. 13. The 6t3C and 6’*0 values (%) for significant species from subcore 8-l are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (8) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each taxon are also indicated. Some deep infaunal occurrences are due to turbidite burial of an epifaunal assemblage (see text for discussion).
South China Sea Core 3 (1095 m) (52~PDW
Fig. 14. The 8r3C and 6’*0 values (?&I)for significant species from subcore 3-2 are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (8) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each taxon are also indicated.
1633
1634
A. E. Rathbum et al. Average Stable Isotope differences
sea
suhl
SouthChina Sea A S’“0
A S’*O -1
0
1
-2
2
-4
-1
0
1
.
.
A 6°C -1
0
1
A
0
-2
6°C 0
2
spp.
(E) Clbkklokka Clbkklddes bdyl
6) DW
pro*
(Tl &Gddddw bndyl 0 Mekloak amoh 0 Drldmnlk umbonntm (S) Url&ns Prdmncidu (8 Bulimha medana
Fig. 15. Average values for the difference between test gL80 values and equilibrium calcite 6’*0 (AS’*O), and for the difference between test 6% values and ambient bottom-water 613C(AS”C), for each taxon represented by more than a single isotope analysis. The 6’*0 for equilibrium calcite for the bottom-water (S’sO,,) at each site was calculated as described in the text, and subtracted from the g’s0 values for specimens analysed from each core. The 6% values of each taxon represented by more than a single isotope analysis was subtracted from the estimated bottom-water 613C(6’3C b,w.) at each site. The average isotopic difference for each taxon was computed and plotted along with the standard deviation. As plotted, g’sO,.,. and 8’3Cb.W.=O. Note that the unusual 6”O and 613Cvalues of -0.71% and - l.O%, respectively, for S. reticuluta at 0-l cm in core 8 were not included in the average or standard deviation calculations (see Table 3 and Fig. 15). Species labeled with an asterisk, *, have an aragonitic test. Microhabitat preferences are delineated by the following symbols: E, epifaunal; T, transitional; S, shallow infaunal; D, deep infaunal.
These calculated values (Table 1) are within the expected range of 613C values based on GEOSECS 613C data and the results reported by McCorkle and Keigwin (1994). We believe that our estimates are correct to within 0.2%0.Despite slightly higher dissolved oxygen levels in the South China Sea, bottom-water 613C values are more negative than those of the Sulu Sea because of the differences in water temperature and oxygen solubility (and AOU) of the bottom-waters of these basins. The differences between bottom-water 613C estimates and the measured 613C values of benthic foraminiferal specimens at each site are calculated and reported as A6r3C values. Average A6r3C and A6r8O values for each South China Sea and Sulu Sea taxon which is represented by more than one stable isotope analysis are presented in Fig. 15.
Standing stocks Results from this study yield standing stocks from 2982 to 66150 cm2 in the Sulu Sea and 2967 to 239150 cm2 in the South China Sea, and are within the range of values reported for other regions (Table 1). Total foraminiferal standing stocks are relatively high in the shallower sites in both basins and generally decrease with increasing water depth. The
Ecologyand isotopiccompositionof foraminifera
1635
variability between the 4000 m cores in the Sulu Sea (15 and 16) is probably due to the heterogeneous distribution of siliceous sponge skeletal material (Rathbum and Corliss, 1994). Standing stocks of the calcareous assemblage, which is more representative of the fossil assemblage due to the post-mortem destruction of most agglutinated taxa, also generally decrease with increasing water depth to the deepest site, where standing stocks increase again. The data for core 8 are not considered reliable for standing stocks because of the influence of preserved specimens buried deep within the sediments. While other environmental variables remain relatively uniform in both basins, organic carbon in the sediments generally decreases with increasing water depth, then increases dramatically at the deep sites (Figs 2 and 11). This increase is due to organic carbon transported from shallower regions by turbidites and corresponds to increases in infaunal taxa and subsurface accumulation of organic carbon (Figs 6 and 10). Comparisons of standing stocks reported in other studies are often difficult because of the different size fractions used or because infaunal populations were not sampled. DISCUSSION Generalfaunal characteristics: South China Sea
Agglutinated assemblages dominate the cores and account for a significant portion of the total foraminiferal assemblage. Calcareous assemblages reach maximum densities in the top 1 cm of sediments in both subcores from box cores 3 and 4, while box cores 1 and 2 yielded subsurface density maxima of calcareous assemblages. Densities and diversities decrease with increasing water depth down to 3000 m, below which diversity remains relatively uniform. Densities increase significantly in the 4000 m core due to the additional organic carbon available at the deepest site (Table 1) (the relationship between fauna and organic carbon is discussed below). In the South China Sea, G. lobatulus, Uvigerina species, C. bradyi, C. pacifica, B. cubensis, C. oolina, H. elegans, and 0. culter are common in subcores from 1095 m (core 3), and 0. culter, C. pacljica, Astrononion sp, 0. umbonatus and P. subcarinata are common species in subcores 4-l and 4-2 from 2150 m (Fig. 2). Very few foraminifera are observed in subcores from the 2950m site (core 2), and Cibicidoiaks, Gyroidinoides and Oridorsalis are represented. Subcores from the deepest site (l-l and l-2) are characterized by infaunal populations of C. oolina (Fig. 2). Comparisons with Sulu Sea
The distribution patterns and densities of Sulu Sea species are similar to those in the South China Sea. Agglutinated taxa dominate Sulu Sea cores as they do in the South China Sea sediments, with both calcareous and agglutinate assemblages typically reaching maximum densities in the top 1 cm. Diversity and abundances generally decrease with increasing depth in the sediment and increasing water depth in both basins. In the Sulu Sea Basin, diversity in the deepest core (4515 m) is similar to that in the 4000 m cores, and is probably affected by the greater availability of organic carbon deposited by turbidites; a similar pattern is observed between the 4000 m and the 3000 m sites in the South China Sea (Table 1). In the Sulu Sea, Cibicidoides and Uvigerina are the dominant genera (> 10% of the calcareous assemblage) at 5 10 m (core 12) and together with Siphonina, are also dominant
1636
A. E. Rathbum
et al.
taxa at 1005 m (core 8). Dominant genera at 2000 m (cores 9 and 10) include Gyroidinoides, Oridorsalis, Cibicidoides and, in one core, milioline taxa. The 3000 and 4000 m cores are dominated by C. bradyi and 0. umbonatus, while the most abundant taxon in the deepest core (45 15 m) is the infaunal V. mexicana. The infaunal pattern of V. mexicana is similar to the fauna1 pattern of C. oolina observed in the deepest core of the South China Sea in that both sites are below the lysocline and are interpreted to have been influenced by turbidite sedimentation, with organic carbon brought in from shallower environments. Although differences in dominant taxa exist between basins, the general characteristics of the fauna1 patterns are remarkably similar. Microhabitat preferences
Microhabitat preferences of Sulu and South China Sea taxa have been identified based on vertical distribution patterns and interpretations reported in Rathburn and Corliss (1994) and Tappa (1992) and are summarized in Table 2. In addition to the distribution patterns noted by Corliss (1985, 1991) taxa such as C. bradyi and 0. umbonatus have transitional distributions and are found living from 0 to N 4 cm in the sediments. Taxa which are found in both the Sulu and South China Seas show similar distribution patterns and include C. bradyi, U. proboscidea, H. elegans, and C. oolina. Results from this study support suggestions by Rathbum and Corliss (1994) that Chilostomella is adapted to take advantage of subsurface accumulations of labile organic carbon, even in deep turbiditic sediments near the CCD. South China Sea species which are not common in the Sulu Sea include: the transitional taxa, G. lobatulus and 0. culter, which have maxima at the surface with significant occurrences deeper in the sediments; C. pacz$ca, which has a shallow infaunal maximum from 0-2cm; and B. cubensis, with maximum abundances in deep infaunal (> 4 cm) habitats (Fig. 3). It should be noted, however, that many of the South China Sea taxa, such as B. cubensis, G. lobatulus, and 0. culter, are found primarily in core 3, which may be significantly affected by bioturbation. The morphologies of most taxa are related to their microhabitats, as discussed by Corliss (1985,1991), Corliss and Chen (1988), and RathbumandCorliss (1994). Theplanoconvex to biconvex morphologies of G. lobatulus and 0. culter, however, are considered epifaunal attributes(Corliss, 1985,1991;CorlissandChen, 1988),butthesetaxaarealsofoundwithinthe sediments in core 3. Large numbers of epifaunal taxa occur in the 13-14 cm interval in Sulu Sea core 8, and Rathburn and Corliss (1994) interpreted this occurrence as a preserved epifaunal assemblage that was buried by turbiditic sedimentation. No buried epifaunal assemblage was observed in core 3. Occurrences of stained fauna deep within bioturbated sediments, however, is consistent with observations in the Skagerrak, where Corliss and van Weering (1993) reported complex distribution patterns of benthic foraminifera in bioturbated, organic-rich sediments. These infaunal patterns were attributed to heterogeneity in subsurface environments due to a relatively high amount of biological activity. Variables influencing fauna1 patterns
Environmental variables such as temperature (e.g. Polski, 1959; Phleger, 1960; Biswas, 1976), organic carbon (e.g. Lutze, 1980; Miller and Lohmann, 1982; Lutze and Coulboum, 1984; Corliss and Chen, 1988; Caralp, 1989; Corliss and Emerson, 1990; Herguera and Berger, 1991) and bottom-water oxygen (e.g. Lohmann, 1978; Schnitker, 1979; Burke, 1981;
Ecology and isotopic composition of foraminifera
1637
Perez-Cruz and Machain-Castillo, 1990; Kaiho, 1991, 1994) have been suggested to significantly influence some species of benthic foraminifera. The relatively uniform bottom-water oxygen and temperature conditions within the Sulu and South China Seas combined with the contrasting bottom-water properties of these basins make this an excellent area in which to compare fauna1 assemblages and examine the variables which influence benthic foraminiferal distribution patterns. Temperature
Significant differences exist in dominant taxa (2 > 10% of calcareous fauna) in the > 150 pm fraction between the thermospheric Sulu Sea Basin and the psychrospheric South China Sea basin as shown in Fig. 2. Gavelinopsis, Bolivinopsis, Astrononion, Osangularia, and Ceratobulimina are common taxa in the South China Sea but are rare to absent in Sulu Sea sediments. Siphonina and Valvulineria are dominant taxa at certain depths in the Sulu Sea, but are absent in South China Sea samples. Since other environmental variables are similar between basins, these differences in dominant taxa are suggested to result from the large differences in bottom-water temperatures. Differences in selective predation, specific food requirements, and recruitment may also influence fauna1 distributions, but the proximity of the basins indicates that these factors are not primary controls of the observed patterns. Although fauna1 changes are evident within each basin, temperature does not vary significantly below 1000 m within the Sulu Sea and South China Sea basins (Table l), suggesting that bottom-water temperature cannot account for the fauna1 changes observed within each basin. The evidence for the influence of temperature as a controlling factor is limited, as the South China Sea data is based primarily on one core 3, and differences occur between sites within each basin. Nevertheless, the large difference in temperature between the basins seem to influence the distribution of some taxa. Bottom-water oxygen
Although dissolved bottom-water oxygen content has been ascribed as a primary factor controlling some species of benthic foraminifera (e.g. Lohmann, 1978; Burke, 1981; PerezCruz and Machain-Castillo, 1990), results from this study do not support this assertion. Many of these species which have been suggested to be associated with low-oxygen conditions, such as Bolivina and Bulimina, are present in the shallow sites of the Sulu Sea but do not occur in significant numbers in deeper water despite the similarity of bottom-water oxygen levels (Rathburn and Corliss, 1994). Comparisons of living assemblage distributions with core-top dead assemblages indicate that the absences of these “low-oxygen taxa” are not due to seasonal variations or recent flushing of the Sulu Basin (Rathbum and Miao, 1995). In the South China Sea, bottom-water oxygen levels are also quite low (up to about 1.8 ml l-l), and only slightly higher than those of the Sulu Sea sites, increasing by > 0.5 ml 1-l from 1000 m to 4000 m (Fig. 2). The > 150 pm fraction data and a qualitative examination of the 63-150 l.un fraction in South China Sea samples do not reveal high numbers of “low oxygen taxa” such as Bolivina and Bulimina. Organic carbon
Organic carbon has been suggested to be an important influence on the abundances and distribution patterns of deep-sea benthic foraminifera, including those in the Sulu Sea (Rathburn and Corliss, 1994). The South China Sea data are consistent with these observations, although it is difficult to assess the distributions of smaller taxa, such as
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Bolivina, without quantitative data on the 63-150 pm fraction. Taxa such as Uvigerina, Bulimina, Bolivina, and Chilostomella, which have been associated with high organic carbon
environments in the Sulu Sea (Rathburn and Corliss, 1994), have similar distributions in the South China Sea. Uvigerina, Bulimina, and Bolivina are most abundant in the shallowest cores (510 and 1005 m: Sulu Sea; 1095 m: South China Sea), but are not abundant in deeper sites where organic carbon values are lower. In contrast to living (this study) and fossil data from samples off the northwestern coast of Palawan, fossil material from the surficial sediments of gravity cores taken in the South China Sea off the southwestern coast of Palawan yielded significant percentages of Bolivina and Bulimina (Miao and Thunell, 1993). Since the bottom-water properties (oxygen content, temperature, and salinity) of the southwestern South China Sea are similar to those of our South China Sea study area, but organic carbon values of the sediments are significantly higher (0.84-2.22%), occurrences of these taxa appear to be related to the presence of organic carbon in the sediments in the South China Sea as well as the Sulu Sea. The infaunal species, Chilostomella oolina, is abundant in sediments from 1095 and 3980 m in the South China sea and 510, 1005 and 4515 m in the Sulu Sea where subsurface organic carbon levels are higher (> 0.74%) (Figs 3 and 11). The relatively high organic carbon contents found in the deepest core from each basin are interpreted to result from turbiditic sedimentation. The occurrence of high-abundance, low-diversity assemblages dominated by C. oolina in the deepest core of the South China Sea is consistent with the idea that Chilostomella is able to take advantage of subsurface accumulations of organic carbon in abyssal turbiditic sediments. Although surficial organic carbon levels are higher in the deepest sites than at shallower depths of both basins, surficial sediments in the deepest cores (South China Sea core 1: 3980m and Sulu Sea core 18: 4515m) are inhabited almost exclusively by agglutinated taxa. The corrosivity of bottom waters (CCD is 3800-4000 m in the South China Sea; 45004800 m in the Sulu Sea) may prevent many calcareous taxa from inhabiting the top 2-5 cm of sediments in deeper portions of these basins. Calcareous species that prevail under these conditions are those which are adapted to the low-oxygen environments deeper in the sediments where labile organic carbon is available. These deep-dwelling specimens can be preserved in the geologic record of these areas (see Resig, 1981 and Miao, 1993) and more work is needed on these environments. Standing stock
Total foraminiferal standing stocks generally decrease with increasing water depth, although standing stocks for calcareous taxa increase in the deepest cores of both basins (Table 1). Previous studies have reported wide ranges in the standing stocks of deep-sea foraminifera (e.g. Coull et al., 1977; Thiel, 1979, 1983; Snider et al., 1984; Gooday, 1986; Alongi, 1987; Mackensen and Douglas, 1989; Silva et al., 1996). Comparisons between studies are often difficult because of the different methodologies and sieve sizes used, but Gooday (1986) noted that deep-sea foraminiferal standing stocks are typically reported as being lower than 1000 per 50 cm2. Except for the three shallowest sites (cores 12,8, and 3), all of the cores in the study area fall below 1000 specimens per 50 cm2 in the > 150 pm size fraction (Table 1). When the 63-150 pm fraction is also included, however, cores 9, 10 and 20 yield densities close to 1000 specimens per 50 cm2. In this study, higher organic carbon contents generally yield higher standing stocks within a given basin, but increases in standing stocks are not necessarily proportional to the
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corresponding increase in organic carbon. There is a general relationship between relative suticial organic carbon contents and fauna1 abundances within a basin, but the number of specimens per milligram organic carbon ratio is not consistent between basins. A number of studies have suggested that deep-sea macrofaunal and meiofaunal standing stocks are directly related to food availability (see Thiel, 1983 and Jumars and Wheatcroft, 1989 for reviews). Previous workers have noted, however, that organic carbon contents of deep-sea sediments correlate only approximately with biomass values and that better correlations are obtained with parameters more closely related to primary productivity such as chlorophyll (Pfannkuche and Thiel, 1987; Altenbach and Sarnthein, 1989) and phytodetrital flux (Gooday, 1988; Gooday and Lambshead, 1989; Altenbach, 1992). Different components of organic carbon may provide direct (Caralp, 1989; Delaca, 1982; Delaca et al., 1980,198 1) or indirect food sources (Langer and Gehring, 1993; Goldstein and Corliss, 1994) for different foraminiferal species, and some varieties of organic carbon may not be available as food sources for foraminifera. The correlations between fauna1 patterns and surficial and turbiditic subsurface organic carbon values in this study indicate that there are differences in the quality of organic carbon as a food source for benthic foraminifera, as suggested by other workers (Caralp, 1989; Altenbach and Sarnthein, 1989; Gooday and Turley, 1990; Gooday et al., 1992; Rathbum and Corliss, 1994). The lack of a direct relationship between population densities and organic carbon values in this study also indicates that other factors such as the quality of organic carbon influence foraminiferal standing stocks (e.g. Lipps, 1983; Gooday and Turley, 1990). Stable isotope compositions Carbon isotopes
The 613C data generally support the suggestion that the carbon isotopic composition of benthic foraminifera is influenced by microhabitat preferences. In typical deep-sea sediments, pore-water 613C decreases down core as a result of the oxidation of organic matter rich in I2C (McCorkle et al., 1985, 1990; Sackett, 1989). The 613C pore-water gradient is reflected in the carbon isotopic composition of taxa living on and within the sediments; epifaunal species have the highest values and are closest to equilibrium with the overlying bottom-waters, while infaunal taxa have lower 613C values which are related to the isotopic values of pore-waters (McCorkle et al., 1990). In this study, epifaunal taxa such as C. wuellerstorji, C. pachyderma, and Cibicidoides spp. typically have the highest 613C, deep infaunal species such as C. oolina have the lowest values, and transitional and shallow infaunal taxa such as G. subglobosa, U. probosidea, and B. mexicana have intermediate values (Figs 12-15). These data are consistent with the idea that microhabitat preferences influence the carbon isotopic composition of individual species. Vital effects are indicated, however, for the deep infaunal species, B. cubensis, whose 613C values are not consistent with those of other taxa with similar microhabitat preferences. Although infaunal species typically have lower 613C than epifaunal taxa, B. cubensis has significantly higher carbon isotope values than the epifaunal Cibicidoides spp. Bolivinopsis cubensis constructs a test which is granular in appearance, and the microstructure of the shell material may influence the isotopic values of the test. The differences in isotopic values between B. cubensis and the other taxa in core 3 may reflect interspecific biological differences in fractionating isotopes for shell construction, or may be related to other
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differences between species, such as food preferences. The relationship between the ecological preferences and isotopic compositions of B. cubensis is difficult to assess because this species was abundant in only one core. To our knowledge, this study provides the only isotopic data from representatives of this species. The two aragonitic species in this core also do not conform to the pattern seen in calcitic species. Gavelinopsis lobatulus has a transitional microhabitat preference, but has lower 613C values than deep infaunal taxa in core 3, whereas the shallow infaunal species, C. pac$ca, has significantly higher carbon isotope values than the epifaunal Cibicidoides spp. Grossman (1984a,b, 1987) and Grossman and Ku (1986) observed that the 613C values of aragonitic tests can be influenced by bottom-water temperatures, while no such effects were suggested for the 613C of calcitic taxa. Temperature effects may influence the 613C values of G. lobatulus and C. pacljica but cannot account for the large differences between these species. Note that H. elegans yields carbon isotope values that conform to the pattern of relatively high 613C for epifaunal taxa, but which are also consistent with the relatively high values reported for this aragonitic species by previous authors (e.g. Grossman and Ku, 1986; McCorkle et al., 1990). Plots of average A613C values for each taxon represented by multiple stable isotope analyses show patterns similar to those observed by McCorkle et al. (1990) (Fig. 15). Epifaunal taxa such as C. pachyderma and Cibicidoides spp. tend to have higher A613C values relative to transitional and shallow infaunal species, with a range of about 2%0.The deep infaunal C. oolina has a low A613C value compared to epifauna, shallow infauna and transitional species, but is only about 2% lighter than equilibrium calcite as compared with the - 4% A613C values of Chilostomella reported by McCorkle et al. (1990). The aragonitic species, H. elegans and C. pacifica, have high A613C values as expected, but the aragonitic taxon, G. lobatulus, has an unexpectedly low A613C value, and the deep infaunal species, B. cubensis, has an unexpectedly high Ac1613C value for a calcitic species. Previous studies report 613C values of 0. umbonatus as significantly lower and more variable than those of C. wuellerstor- (Woodruff et al., 1980; Belanger et al., 1981; Graham et al., 1981; Berger and Wefer, 1988). The transitional infaunal (0-4cm) microhabitat preference of 0. umbonatus documented in the Sulu Sea cores (Rathburn and Corliss, 1994) is reflected in lower A613C values (Figs 12-15, Table 3), which can account for the “anomalous” isotopic values noted in previous studies. This study did not find high variability in the A13C values of 0. umbonatus, but the eurytopic lifestyle of this species could also account for variability in carbon isotopic composition. Carbon isotopes of taxa found in the same interval
The range in 613C for specimens from the same interval within a core may be substantial (about -l&1.6% in core 12; -3.&0.3°h for core 8; - 1.3~.2s/oo for core 10; and -0.80.0%0for core 20), but within these intervals taxa identified as epifaunal from this and other studies have higher 613C than infaunal taxa (Fig. 12). Except for 0. umbonatus in core 20 and U. peregrina in core 3, most taxa found over a depth range within the sediments do not show consistent gradients in 613C as would be expected if carbon isotopic compositions were influenced only by the average pore-water environments where they were found. Differences in isotopic compositions between living (stained) benthic foraminifera taken from the same interval as seen in this study and in previous studies (Woodruff et al., 1980; Grossman, 1984a, b; McCorkle et al., 1990; Loubere et al., 1995) can be explained by: (i)
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vertical movement of infaunal taxa within the sediments, with species secreting all or portions of the test in deeper sediments; (ii) differences in food preferences; (iii) vertical mixing of specimens by bioturbation; (iv) vital effects (differences in isotopic fractionation due to inherent biological processes); (v) microenvironments within the 1 cm sample interval; or some combination of these explanations. These explanations also have to account for both the consistency of 613C compositions of taxa within the sediments and observed distribution patterns. Seasonal vertical movements of some deep-sea benthic foraminifera have been reported in the northeastern Atlantic (Gooday, 1988) and the Adriatic Sea (Jorissen et al., 1992), but not in the California borderlands (Silva et al., 1996). Given that burrowing is the most energy-consuming mode of movement (Jumars and Wheatcroft, 1989) it would be highly inefficient to consume food near the surface (such as in core 12) and burrow deeper to secrete CaC03. This is especially true in environments like the deep-sea, where food availability may be periodic and where opportunistic behavior may prevail. Ontogenetic changes in sediment-depth preferences are possible, but fauna1 results from different size fractions in the Sulu Sea suggest that this is not likely (Rathburn and Corliss, 1994). Food partitioning has been reported in other meiofaunal populations (Carman and Thistle, 1985), and since food sources can affect the carbon isotopic signals of organisms (Sackett, 1989; Wefer and Berger, 1991) it is possible that food preferences may contribute to differences in isotopic compositions of foraminiferal species found in the same interval. Food preferences are likely to be related to microhabitat preferences and could also account for the consistency of isotopic compositions of each species over a range of depths within the sediment. In addition to the possibility of a direct influence of food on foraminiferal shell chemistry, differences in food preferences could be an indirect influence by causing species to congregate near micro-food sources; similar organic food sources might generate similar pore-water microenvironments (see discussion below). The effects of food preferences on the isotopic compositions of benthic foraminifera, however, have not been examined. Mixing by macrofaunal bioturbation may vertically transport individuals in the sediment. The mixing of foraminifera from different sediment depths by bioturbation could account for the consistency of isotopic signals within a taxon and for the interspecific isotopic differences between specimens from the same interval. Bioturbation, however, cannot account for the distribution patterns of benthic foraminifera within the sediments (e.g. Corliss and Emerson, 1990). McCorkle et al. (1990) show that the carbon isotopic compositions of benthic foraminifera are significantly influenced by the microenvironments where they live. Bioturbated individuals may stop growing after being transported to a marginal habitat, and the 613C composition of their tests should, in part, reflect the microhabitat in which they prefer living (where their tests were secreted). Although a few individuals may live in marginal microhabitats to which they have been transported, the occurrence of significant numbers of specimens within the sediments examined suggests that these sediment intervals are within the microhabitat range of the taxa represented. If these taxa are living within their optimal microhabitat range, mixing may account for the occurrence of some individuals within the sediments but cannot explain the isotopic variation between species occurring in the same interval. Microgradients in deep-sea sediment properties have been reported (e.g. Aller and Aller, 1986), and heterogeneity in microhabitats may affect the 6i3C value of benthic foraminfera tests (McCorkle et al., 1990; Loubere et al., 1995). The sediment depth ranges for many
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benthic foraminiferal taxa overlap (e.g. epifaunal, O-l cm; shallow infaunal, O-2 cm), and as a result, species that are categorized as having different microhabitat preferences may be found in a single sample (the same interval). The isotopic composition of each species generally agrees with its microhabitat preference, even when different species with different preferences are found in the same interval; epifaunal taxa have higher 613C values than shallow infaunal and transitional species (Fig. 12). In deeper sediment intervals, shallow infaunal and transitional taxa have higher values than deep infaunal taxa (e.g. Fig. 13). Since this isotopic ranking of species within the same sediment interval agrees in general with microhabitat preferences, we suggest that fine-scale heterogeneity of microenvironments within the intervals sampled accounts for this correlation and that the isotopic compositions of most taxa are related to the microhabitats where they secrete their tests. Intrageneric differences
Intrageneric isotopic differences are evident in Cibicidoides and possibly Uvigerina and Bulimina. Cibicidoides bradyi is a transitional taxa, living in sediment depths from O-4 cm, and C. wuellerstorfi (Planulina wuellerstorji) is an epifaunal species (Corliss, 1985, 1991), preferring a microhabitat elevated above the sediment-water interface (Lutze and Thiel, 1989). The 613C value of C. wuellerstorfi in core 10 is higher than those of C. bradyi, as would be expected based on their different microhabitat preferences (Table 3). The 613C of B. marginata (- 0.58%) and B. mexicana ( - 1.08%) from the same interval of core 12 indicate that there may be intrageneric differences among Bulimina species. If the 613C values with standard deviations > 0.05 of U. peregrina and U. proboscidea from the same surficial intervals in cores 12 and 3 are reliable (marked in parentheses in Table 3), there are intrageneric differences of at least 0.1-0.2X in Uvigerina. Oxygen isotopes
Average differences between 6i8O values of Sulu and South China Sea taxa and the 6’*0 at equilibrium with calcite in the surrounding bottom-waters are generally consistent with those reported in previous studies. The range of Aa’* in calcitic species from the Sulu and South China Seas is about 1.OL (Fig. 15). In the Sulu Sea, B. mexicana, 0. umbonatus, and U. proboscidea are closest to equilibrium with calcite (within 0.3X). Chilostomella oolina and U. Peregrina have average 6’*0 values within 0.3% of equilibrium calcite in the South China Sea. The relatively large standard deviation of C. pachyderma 6’*0 values results from the inclusion of the value from the 2.5-3 cm interval (the isotope value from this interval seems unusually high, but we saw no reason to exclude this measurement). Comparisons of the A6180 values of the two species which occur in more than one sample in both Sulu Sea and South China Sea isotopic data sets reveals that C. bradyi and U. proboscidea may have slightly higher Aal values (by about 0.2%) in the Sulu Sea. In each basin, however, these species have A.6180 values which are separated by about 0.1% (difference = 0.13 in the Sulu Sea, and 0.09 in the South China Sea). South China Sea species have As’*0 values which may be related to microhabitat preferences, but in contrast to the patterns noted by McCorkle et al. (1990), Sulu Sea data exhibit no trends in Ag’*O associated with microhabitat preferences. In the Sulu Sea, the aragonitic taxon, H. elegans, is enriched by about 0.4-0.6%0 in 6180 relative to Uvigerina species, and similar differences have been noted in previous studies (e.g. Grossman and Ku, 1986; McCorkle et al., 1990). In the South China Sea, the aragonitic taxon, C. paczjica is enriched by about 0.2-0.04%0
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relative to Uvigerina species, whereas G. lobatulusis depleted by about 1.2%0 relative to Uvigerina.This significant depletion in the al80 of G. lobaruh is unusual for an aragonitic taxon, but because of the lack of isotopic data for this species in other areas, comparisons are not possible. Acknowfedgements-We thank the crew and scientists aboard the R.V. Moanu Wavefor assistance during the Sulu Sea-South China Sea Cruise; E. Tappa, A. Bruce, K. Hicks, Aimee Dolan-Laughlin, M. Malone, M. Qingmin, and M. Fay for technical assistance; R. C. Thunell, T. C. Johnson, D. A. Livingstone, and P. A. Baker for examining an earlier version of the manuscript. Comments and suggestions included in the reviews by D. McCorkle and E. Grossman significantly enhanced the paper. We are grateful to M. Rutgers van der Loeff for providing pore-water oxygen data and to S. Kuehl and T. Fuglseth for providing sedimentation rate and mixing coefficient data. Helpful discussions with D. McCorkle, B. Opdyke, and M. Malone are also very much appreciated. Many thanks are due to Patrick De Deckker and the Australian Marine Quatemary Program in the Geology Department at the Australian National University for their support and hospitality during the senior author’s recent postdoctoral work in Canberra, Australia. This research was supported by National Science Foundation Grants OCE-8700744 and OCE-90-12581.
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Jumars P. A. and R. A. Wheatcroft (1989) Responses of benthos to changing food quality and quantity, with focus on deposit feeding and bioturbation. In: Productivity of the ocean: past andpresent, W. H. Berger, V. S. Smetacek and G. Wefer, editors, John Wiley and Sons, New York, pp. 235-253. Kaiho K. (1991) Cenozoic changes of Paleogene aerobic/anaerobic benthic foraminifera and deep-sea circulation. Palaeogeography, Palaeoclimatology, Palaeoecology, 83, 6585.
Kaiho K. (1994) Benthic foraminiferal dissolved-oxygen index and dissolved levels in the modem ocean. Geology, 22, 719-722.
Kroopnick P. M. (1985) The distribution of “C of XC02 in the world oceans. Deep-Sea Research, 32, 57-84. Kuehl S. A., T. J. Fuglseth and R. C. Thunell (1993) Sediment mixing and accumulation rates in the Sulu and South China Seas: Implications for organic carbon preservation in deep-sea environments. Marine Geology, 111, 15-35.
Langer M., L. Hottinger and B. Huber (1989) Functional morphology in low-diverse benthic foraminiferal assemblages from tidal flats of the North Sea. Senckenbergiana Maritiarna, 20, 81-99. Langer M. R. and C. A. Gehring (1993) Bacteria farming: A possible feeding strategy of some smaller, motile foraminifera. Journal of Foraminiferal Research, 23, 4W6. Linsley B. K., R. Thunell, C. Morgan and D. Williams (1985) Oxygen minimum expansion in the Sulu Sea, western equatorial Pacific, during the last glacial low stand of sea level. Marine Micropaleontology, 9, 395-418. Lipps J. H. (1983) Biotic interactions in benthic foraminifera. In: Biotic interactions in Recent and fossil benthic communities, M. J. S. Tevesz and P. L. McCall, editors, Plenum Press, New York, pp. 331-376. Lohmann G. P. (1978) Abyssal benthic foraminifera as hydrographic indicators in the western South Atlantic. Journal of Foraminiferal Research, 8, 6-34.
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Deep-Sea Research I, Vol. 43, No. 10, pp. 1617-1646,1996 Copyright Q 19% Elsevicr S.zieaceLtd Printed inGreatBritain. AU rights mened S0967-0637@6)00071-4 0967-0637/96$15.00+0.00
Comparisons of the ecology and stable isotopic compositions of living (stained) benthic foraminifera from the Sulu and South China Seas A. E. RATHBURN,*$ B. H. CORLISS,* and K. C. LOHMANNt
K. D. TAPPA*
(Received 28 April 1995; in revisedform 20 March 1996; accepted 26 April 1996)
Ah&act--Significant differences are observed between living (Rose Bengal stained) deep-sea benthic foraminifera found in 14 box cores (510-4515 m) from the thermospheric (> 10°C) environments of the Sulu Sea and the psychrospheric (< 10°C) conditions in the South China Sea. Gavelinopsis, Bolivinopsis, Astrononion, Osangularia and Ceratobulimina are common taxa in the South China Sea, but are rare to absent in the Sulu Sea; Siphonina and Valvulineria are dominant genera at certain depths in the Sulu Sea, but are rare to absent in the South China Sea. Fauna1 differences appear to result from large differences of the bottom-water temperatures (differences from about 6 to 8’C) between these basins. Fauna1 abundance patterns within each basin are suggested to be related to the organic carbon contents in the sediments, since temperatures, salinities and dissolved oxygen levels of the bottom-waters are relatively uniform. The 8’*0 values show a > 2%~range and are similar to those presented by previous workers, but have no consistent relationship with microhabitat preferences. Vertical distribution patterns and carbon isotope compositions of species, however, reflect microhabitat preferences and are consistent with previous observations from other regions. Epifaunal species (O-l cm interval) such as Cibiciakndes pachyderma, Ctbictdoiaks wuellerstorf, Hoeglundina elegans and Anomalinoides colligera, have higher 813Cvalues than taxa which have the ability to live deeper within the sediments. Infaunal taxa that live in the upper 2-3 cm, including Uvigerina peregrina, Uvigerina proboscidea, and Bulimina mexicana, have lower 6°C values than epifaunal species, and the deep infaunal species, Chilostomelia oolina, has the lowest 6% Cibicidoides bradyi and Oridorsahs umbonatus are found between 0 and N 4 cm and have lower carbon isotope values (by > 1.4!%0in some cores) than epifaunal Cibicidoides species. Exceptions to this pattern include the aragonitic species, Gavelinopsb lobatulus, (0-4cm) which produces significantly lower 813C values than deep infaunal taxa, and the shallow infaunal species, Ceratobulimina paczfica (also aragonitic) and Bolivinopsis cubensis (deep infaunal), which yield higher carbon isotopic values than epifaunal taxa. These exceptions are found primarily in only one core, and additional samples are needed to confirm the relationship between their distribution patterns and isotopic compositions. Each of the species examined has a relatively consistent 813C value throughout its distribution within the sediments that may result from heterogeneity of microhabitats within the intervals sampled. Intrageneric differences in 8% of Cibicidoiaks, and possibly Uvigerina and Bulimina, are evident. The isotopic differences between C. bradyi and many other Cibicidoides species are related to differences in microhabitat preferences between species. The 8i3C results confirm the influence of microhabitat preferences on the carbon isotopic composition of deep-sea benthic foraminifera and reaffirm the importance of assessing the microhabitat preferences of species used for isotopic analyses. Copyright 0 1996 Elsevier Science Ltd
*Department of Geology, Duke University, Durham, NC 27708, U.S.A. 7 Department of Geological Sciences, University of Michigan, Ann Arbor, MI 48109-1063, U.S.A. $Present address: Scripps Institution of Oceanography, Marine Life Research Group, 9500 Gihnan Drive, La Jolla, CA 92093-0218, U.S.A. 1617
1618
A. E. Rathbum et al.
Fig. 1. Regional map of the study area with Western Caroline Basin cores plotted and bathymetric map of the Sulu and South China Seas inset area showing box core locations. Depth contours in meters.
INTRODUCTION Distribution patterns of deep-sea benthic foraminifera and the stable isotopic compositions of their tests have been extremely useful as indicators of paleoceanographic conditions. In order to accurately infer ancient bottom-water conditions from fossil benthic foraminifera, we must understand the factors which influence the distribution of benthic foraminifera and determine the relationships between foraminiferal shell chemistry and environmental and ecological parameters. The uniform bottom-waters of the Sulu Sea and the contrasting bottom-water properties of the adjacent South China Sea furnish a natural setting for a comparative study of the ecology of benthic foraminifera and the geochemistry of their shell material. Observations on the ecology and isotopic composition of species living in these basins can be applied to the interpretation of fossil assemblages from a variety of settings in the world ocean. This paper focuses on (i) comparisons of fauna1 distribution patterns in the warm ( > 1O’C) Sulu Sea with those found in the cooler South China Sea; and (ii) the relationships between benthic foraminiferal stable isotope compositions and microhabitat preferences.
STUDY
AREA
Sulu Sea
Located between the Philippine Islands and Sabah (Borneo), the Sulu Sea is an isolated marginal basin (250,000 km2), surrounded by sills which are generally less than 200 m deep (Exon et al., 1981) (Fig. 1). South China Sea intermediate water flows through a single 420 m deep channel in the Mindoro Strait, providing the only source of deep water to the Sulu Sea basin (Van Riel, 1943; Wyrtki, 1961; Frische and Quadfasel, 1990). As a result, the Sulu Sea is a thermospheric (> 1O’C) basin with uniform salinities (- 34.5), warm temperatures (- lO.S”C), and low dissolved oxygen values (- 55 pM x 1.25 ml 1-l) in water depths below
1619
Ecology and isotopic composition of foraminifera SOUTH CHINA SEA (4
(b)
‘J
TEJWRRATURE
(‘Cl
SUL.U SEA
_ -11
SOUTH CHINA SEA
DISSOLVED OXVGRN (mL’L)
SULAJ SEA
*.,s -
Fig. 2. Schematic drawing showing: (a) temperature distribution in the South China Sea and Sulu Sea; surlicial organic carbon, schematic core depth distribution and dominant genera (> 10% of calcareous assemblage) for the > 150 pm and > 63 pm fractions are also plotted. Parentheses refer to taxa which comprise > 10% of the calcareous assemblage in one subcore, but not in the duplicate subcore; (b) oxygen distribution in the South China and Sulu Seas.
1000 m (Fig. 2 and Table 1). The aragonite compensation depth is at 1400 m, and the calcite compensation depth occurs at 4500-4800 m (Exon et al., 1981; Linsley et al., 1985). Surfkial sediment organic carbon contents ranged from > 0.10% to > 2.5%; the highest values
1620
A. E. Rathburn er al.
Table 1. Core locations, water depth (m), number of taxa, standing stocksfor > 150 pm and > 63 pmfractions (no. per 50 cm2), bottom-water oxygen levels (@I), temperatures (“C), salinities (V&I), calculated 6”O of equilibrium calcite (S’80,,,(~PDB)), and calculated 6’3C of the ambient bottom-water (613Cb.,,(%PDB)) (see text for discussion)
Standing stock (No. per 50 cm2) > 150pm >63pm CO=
Depth
Sulu Sea 12 510 8
1005
Lat. (‘NJ
Long.
(“E)
Total
TOtal
TOtal
Total
No.
01
Temp.
foram.
talc.
foram.
CA.
SPP.
(PM)
(“C)
2416
1237
II2
8” oz.!?
118” 22.4
1305
437
8” 08.5
118” 35.0
2982
1063 II58
Sal. %n
6’80 cc.
S’=O b.w.
K
?fa
78.5
11.06
34.46
1.38
73
71.8
10.10
34.45
1.61
-0.03
0.06
10
1980
8” 20.6’
118” 57.6
605
84
322
49
57.2
IO.15
34.46
1.60
-0.15
9
1995
8” 20.6
118” 57.9
612
137
964
278
39
55.9
IO.15
34.46
I.60
-0.15
20
3000
6” 54.5
119” 10.0
557
44
937
110
32
53.8
10.29
34.41
1.56
-0.15
15
3995
7” 33.9
120” 19.8
66
II
88
I3
IO
54.6
10.46
34.47
I6
4000
7” 32.9
120” 19.5
472
21
145
55
13
53.8
10.46
34.47
18
4515
7” 25.3
121” 12.5
110
I75
199
I4
53.6
10.54
34.47
2046
639
44
89.1
4.19
3.11
- 0.20
316
59
20
103.2
2.48
109.3
3.56
-0.16
II9
South China Sea 3
1095
10” 57.3
118” 27.5
4
2150
I I” 53.3’
llE”20.4
2
2950
12” 07.1’
118” 03.6
162
7
6
I
3980
13” 36.5
117O41.2
584
70
6
2.45 2.46
Western Caroline Basin 23
3025
7” 37.1’
138” 47.7
84
I9
22
3515
7” 18.6
138” 11.0
40
I6
165
86
19
146.4
1.60
34.67
I5
156.9
1.50
34.68
occurred between 500 and 1200 m, and the lowest values were found on the western shelf and in the central basin. Organic carbon values > 1% were found in turbidites below a depth of 4500 m (Exon et al., 1981). South China Sea Located immediately west of the Sulu Sea, the South China Sea is also a semi-enclosed basin with maximum depths exceeding 5000m (Fig. 1). Bottom-waters are derived from intermediate and deep waters of the Pacific Ocean which flow through the 1900 m deep Bashi Channel in the Luzon Strait (Broecker et al., 1986), located between Taiwan and Luzon (Van Riel, 1943; Wyrtki, 1961). As a result, South China Sea bottom-waters have psychrospheric temperatures of approximately 2.4”C and oxygen levels of over 1.75 ml 1-l x89 uM in the deeper portions of the basin (Fig. 2, Table 1). The aragonite compensation depth of the South China Sea is between 1000 and 1400 m, and the calcite compensation depth is about 38004000 m (Rottman, 1979; Thunell et al., 1992). In the South China Sea area examined in this study, productivity is probably similar to that of the study area in the Sulu Sea. In the study area north of Palawan in the South China Sea, Thunell et al. (1992) and Kuehl et al. (1993) noted that there is no evidence of significant variations in productivity and assumed uniform productivity for the sector. Possible differences in primary productivity of the area are evidenced by higher levels of barite in the sediments of this sector compared with the southeastern South China Sea and the Sulu Sea (Calvert et al., 1993), but organic carbon accumulation data suggest that this is not the case. Organic carbon contents of the sediments increase slightly with depth in this portion of the South China Sea, but there is no evidence of upwelling in this area (Thunell et al., 1992;
Ecology and isotopic composition of foraminifera
1621
Calvert et al., 1993). Upwelling in the Sulu Sea is unlikely due to the hydrography of the basin and the geographic positioning with respect to the prevailing winds (Wyrtki, 1961). As a result, the South China Sea sector examined in this study and the Sulu Sea are thought to have similar primary productivity values ranging from 60 to 100 gC mm2 year (Berger, 1989; Thunell et al., 1992; Kuehl et al., 1993). PREVIOUS
WORK
Benthic foraminiferal distributions
Recent studies of modern benthic foraminifera in the Sulu Sea have noted that the distribution of assemblages is variable within the basin (Exon et al., 1981; Linsley et al., 1985; Rathburn and Corliss, 1994). Based on > 150 pm fraction data from four piston cores and nine surface sediment samples, Linsley et al. (1985) suggested that the faunas are controlled primarily by bottom-water oxygen levels and the quantity of organic carbon. From samples also included in this study, Rathburn and Corliss (1994) demonstrated that living (Rose Bengal stained) assemblages from eight box cores vary with depth, despite the uniformity of bottom-water properties. Rathburn and Corliss (1994) concluded that the oxygen content in the bottom-water does not control fauna1 distributions, including taxa previously characterized as indicators of low oxygen conditions, and suggested that the benthic faunas are influenced by the organic carbon content of the sediments. The influences of bottom-water oxygen concentrations and organic carbon on benthic fauna will be considered in detail later in this paper. The relatively few studies that have focused on recent benthic foraminifera in the South China Sea include those of Polski (1959) in the East China and Yellow Seas, Biswas (1976) on the Sunda Shelf, and Waller (1960) along the western margin of the South China Sea. Miao and Thunell(1993, 1995) examined benthic foraminifera from gravity cores taken in the Sulu and South China Seas and concluded that organic carbon and oxygen penetration depth affect the distribution of benthic foraminifera in both basins. Stable isotope studies
Intraspecific and interspecific differences in stable isotopic compositions of benthic foraminifera have been documented by a number of researchers, and both positive and negative correlations between 6i3C and al80 have been reported (e.g. Duplessy et al., 1970; Woodruffet al., 1980; Belanger et al., 1981; Graham et al., 1981; Grossman, 1984a,b, 1987; Mackensen and Douglas, 1989; McCorkle et al., 1990). Isotopic differences between benthic foraminifera species have been attributed to various factors, including the incorporation of metabolic products into the test, ontogenetic differences and other “vital effects” (biological differences which result in differences in isotope fractionation), as well as environmental and microhabitat effects (Grossman, 1984a,b, 1987). By comparing glacial and interglacial carbon isotopic values, Zahn et al. (1986) suggested that the 613C values of the infaunal “Uvigerina peregrina group” correlated with organic carbon accumulation rates, and carbon isotope values of the epifaunal species, Cibicidoides wuellerstor-, were related to bottom-water isotopic composition. McCorkle et al. (1990) found that 13Ccompositions of epifaunal taxa are related to the isotope values of bottom-waters and that specimens with deeper microhabitat preferences yield lower isotopic signals more closely correlated with
1622
A. E. Rathbum et al.
pore-water isotope values. This correspondence between microhabitat preference and isotopic composition indicates that the carbon isotopic values of benthic foraminifera are at least indirectly influenced by ecological preferences. Interspecific differences between taxa found in the same interval within the cores were also noted, however, indicating that vital effects do exist for some species. METHODS This investigation is based on the analysis of deep-sea benthic foraminifera from 14 Soutar box cores taken on depth transects from 510 m to 4515 m in the Sulu Sea (eight box cores), 1095-3995 m in the South China Sea (four box cores) and two cores (3025 m and 3515 m) from the Western Caroline Basin (Fig. 1, Table 1) collected on the R.V. Moana Wave in August 1988. Subcores (10.1 cm interior diameter clear plastic tubes) were taken from each of these box cores and subsampled in 0.5 cm intervals down to 3 cm, and 1 cm intervals down to 20 cm; each sample was preserved in 4% formalin bu.Bered with Mule Team Borax. For a complete description of the procedures, see Rathburn and Corliss (1994). Oxygen levels, salinities and temperatures in the water column were measured with a Sea Bird profiling CTD equipped with a dissolved oxygen sensor and attached to the box corer, and bottom-waters sampled with Niskin bottles attached to the box corer were also analyzed for oxygen content by Winkler titrations. A minielectrode (Helder and Bakker, 1985) was used to measure the oxygen levels of the porewaters in the sediments of one subcore from each box core except core 1, in which porewater manganese measurements indicate the level of pore-water oxygen penetration (see Rutgers van der Loeff, 1990). Organic carbon weight percentage measurements were made with a Carlo Erba NA 1500 Carbon-Nitrogen-Sulfur Analyzer following the procedure outlined by Lu and Emerson (1987), which is based on methods established by Froelich (1980). In the laboratory, 65 ml Rose Bengal stain solution (1 g 1-i of 4% formalin) was added to each subsample and allowed to stain for at least one week before processing. The sample was then wet sieved using 63 pm and 150 pm sieves. Only the results of the > 150 pm fraction are discussed in this paper. Some Sulu Sea samples were wet-split with a modified Folsom plankton splitter because of the large volume of material in each sample (up to N 100 ml). Each sample was placed in a gridded petri dish with water, and Rose Bengal stained benthic foraminifera were picked from the sample, placed on a micropaleontological slide, identified, and counted. Sulu Sea fauna1 data are based on the analysis of one subcore per box core, whereas South China Sea data are based on two subcores per box core. Species with sufficient specimens for isotopic analyses from subcores 12-2, 8-1, 10-2, 16-2,18-2 in the Sulu Sea and l-2 and 3-2 in the South China Sea were analyzed for carbon and oxygen isotopes at the University of Michigan. All samples were roasted at 380°C and reacted at 73°C with four drops of anhydrous phosphoric acid in a Finnigan MAT carbonate extraction system (“Kiel device”) connected directly to a Finnigan MAT 251 isotope ratio mass spectrometer. Data are reported in the standard 6 notation relative to the Peedee Belemnite (PDB) standard. Precision and calibration of the data were checked with NBS-20 powdered carbonate, and analytical precision was better than 0.1% for both carbon and oxygen isotope analyses. The small volumes of material used for some samples in this study produced variability (standard deviation of > 0.05) in the stable isotope signal detected by the mass spectrometer; these values are marked with parentheses in Table 3 and are not used in the analyses.
Ecology and isotopic composition of foraminifera Table 2.
1623
Microhabitat preferences for selected Sulu Sea and South China Sea taxa
Microhabitat preferences Transitional (O-4 cm)
Epifauna (O-l cm)
Cibicidoides bradyi Cibicidoides robertsonianus Gavelinopsts lobatulus Melonis ajfinis Osangularia culter Oridorsalis umbonatus Siphonina reticulata
Anomalinoides colligera Cibicidoides pachyderma Cibicidoides wuellerstorfi Hoeglundina elegans
Deep infauna ( > 4 cm)
Shallow infauna (&2 cm)
Bolivinopsis cubensis Chilostomella oolina Valvulineria mexicana
Ammonia beccarii Astrononion novozealandicum Bulimina marginata Bulimina mexicana Ceratobuliminapactj?ca Globocassidulina subglobosa Gyroidinoides broeckhiana Pullenia bulloides Trifarina bradyi
Vvigerinaperegrina
RESULTS Vertical distribution patterns of individual taxa, pore-water oxygen content, sedimentary organic carbon, and stable isotope compositions of abundant calcareous taxa are summarized in this section. Fauna1 data (No. per 50 cm3) for the Sulu Sea are given in Rathburn and Corliss (1994), and fauna1 data for South China Sea cores are included in Tappa (1992). Standing stock data from two box cores taken in the Western Caroline Basin are presented in Table 1. Lists of the dominant genera ( > 10% of the calcareous fraction) in the > 150 urn fraction for each core are shown in Fig. 2. Pore-water oxygen data are taken from Rutgers van der Loeff (1990) and unpublished data and information on mixing coefficients and sedimentation rates are from Fuglseth (1991) and Kuehl ef al. (1993). Microhabitat designations are given in Table 2, and carbon and oxygen isotope results are given in Table 3.
South China Sea fauna The > 150 urn fraction of two subcores from each South China Sea box core were examined to assess heterogeneity within a box core. Fauna1 data are plotted with a line connecting the averages of the two subcores at each depth interval (vertical bars represent fauna1 densities from each of the subcores) (Figs 3-6). Differences in abundances of taxa may exist between subcores taken from the same box core, but fauna1 patterns are similar. The microhabitat preferences of dominant fauna are given in Table 2, and fauna1 data from each core is presented in detail in Rathburn (1992); only a few brief comments are included below.
1624
A. E. Rathburn et al.
Table 3. Stable isotopic values (?60 relative PDB) for Sulu Sea and South China Sea taxa. Sample which generated variable isotope signals (standarddeviation of > 0.05) are denoted withparentheses. The number of specimens usedfor each analysis are also included
Sulu Sea Interval
core
Species
613C
South China Sea 6’*0
Number of Specimens
Interval
Species
613C
S’*O
Number of Specimens
12
o-1
A. co&era
-0.17
0.56
5
O-l
A. novozeahmdicum
-0.59
0.52
7
34
B. cubemis
(0.91)
O-l
B. marginolo
-0.58
I .26
7
4-5
B. cubenris
0.87
(1.5) 1.41
22
CL1
B. mexicana
-1.08
1.31
11
5-6
B. cuben&
0.78
1.12
11
&I
C. bradyi
(-0.38)
(1.3)
5
t-7
B. cubenris
0.94
1.31
18
l-l.5
C. bradyi
-0.37
1.06
2
7-8
B. cubensis
0.81
I .22
8
c-l
C. pachydenna
(1.21)
(3.05)
3
a9
8. cubenris
(0.39)
(0.79)
9
I-l.5
C. pochydenna
0.39
0.8
2
9-10
E. c!hnsis
(0.36)
(0.47)
5
34
C. pachyderma
0.38
1.01
2
l&11
8. cubensis
0.92
1.45
9
(0.29)
(I) (1.74)
6
11-12
B. cubenris
0.8
1.29
8
6
1314
B. rubensir
(1.03)
(1.48)
10 7
O-l
c. wut?llerstorji
&I
H. errgaIL
1.55
Core 3 6
l-l.5
H. &gals
1.4
1.78
2
14-15
8. cubensis
0.73
1.13
67
H. ekgans
1.64
1.67
I
I.%16
B. cubensis
0.99
1.28
5
C-l
M. a/fvris
-0.42
0.69
6
16-17
B. cubensis
0.95
1.3
IO
o-l
0. umbonorw
-0.92
1.26
2
17-18
B. cubensis
0.82
1.3
8
1.s2
P. bulioides
-1.3
1.44
4
19-20
B. cubensis
0.9
I .43
13
o-l
S. reticulafa
-0.41
1.02
7
0.51
c. pact@ica
1.46
3.31
7
c-l
CJ. proboscidea
-0.44
1.28
II
1.5-2
c. pqgica
1.3
3.26
2
(-0.58)
(1.38)
3
v. peregrina
O-l core
8
1 l-12
c. pacififo
I .48
3.26
5
67
c. oolina
-1.81
3.06
35 20
45
A. beccarii
-0.11
1.41
2
7-8
c. oolino
(-1.93)
(3.27)
13-14
A. beccorii
(-0.14)
(1.47)
1
O-o.5
C. bradyi
-0.64
2.39
4
&I
A. eolligera
-0.02
0.72
I
0.5-I
C. bradyi
(-0.56)
(2.48)
8
l-l.5
A. co&era
0.11
0.66
1
l-l.5
C. bradyi
-0.59
2.6
2
4-5
A. col@era
0.15
0.78
2
Is-2
C. bradyi
-0.72
2.55
7
&I
B. mexicana
-0.67
1.52
2
O-O.5
Cibicidoides
spp.
-0.01
2.3
3
2-2.5
C. oolino
(-3)
(-0.03)
4
0.5-l
Cibicidoides
spp.
-0.13
2.28
3
7-8
C. oolina
(-2.36)
4
(MS
G. lobaruhu
-3.57
1.61
8
2-2.5
C. pachyderma
(0.28)
(0.2) (0.94)
2
0.5-I
G. lobattdur
-3.42
1.56
6
2.>3
C. pachyderma
I .08
2.18
2
2-2.5
G. lobandw
(-2.69)
(1.67)
2
1314
C. pachyderma
0.34
0.91
3
15-16
G. lobandw
(-3.36)
2
&I
M. affmis
(-0.57)
(1.13)
2
3-l
G. svbxlobosa
(-0.54)
(I .w (2.76)
8-9
h4. aJjjmic
-0.13
0.98
2
12-13
G. subxlobosa
-0.71
2.91
3
O-l
S. rericulara
-1.09
-0.71
4
GO.5
0. c&v
-0.55
2.81
9
2-2.5
S. reticulum
-0.07
1.09
2
SO.5
u. peregrina
-0.72
2.85
4 3
I
2.5-3
S. reticulara
-0.03
1.2
2
0.5-I
u. peregrina
-0.79
2.76
4-5
S. reficulafa
(-0.06)
(1.15)
2
l-l.5
[I. peregrina
(-0.88)
(2.69)
I
5-6
s. rericldara
-0.1
I.15
3
0.5-I
U proboscidea
(-0.58)
(2.71)
3
7-8
S. reticulara
-0.01
1.23
2
3-4
U. proboscidco
-0.34
2.77
5
9-10
s. retic!&ta
(0.35)
(1.67)
2
67
U. proboscidea
-0.41
2.52
6
12-13
S. reticulatrr
-0.1
1.09
2
Core 1
13-14
s. retic!Jara
10
1314 O-1
T. bradyi
(1.36)
2
7-a
c. oolina
-2.39
3.44
(1.93) 1.55
2 2
8-9 %I0
c. oolina
-2.33
3.46
0. umbonarus
(-0.89) -1.12
c. oolino
-2.62
3.49
5
6-7
0. umbonatur
-0.75
1.29
I
10-11
c. oolina
-2.55
3.46
9
12-13
1.46
2
11-12
C. oolina
(0.28)
5
0. umbonlrrur
-0.68
-2.32
3.51
10
O-1
U. proboscideo
-0.28
1.43
4
12-13
c. oolina
-2.47
3.45
8
l-l.5
lJ. probaxidea
2
13-14
C. oolina
-2.42
3.5
9
I.>2
U. proboscidea
(0.06) -0.27
(1.82) 1.37
2
2%3
v. proboscidea
-0.32
1.16
2
8-9
U. proboscidea
-0.28
1.11
3
e10
U. proboscidea
-0.18
1.16
2
11-12
U. proboscidea
(-0.2)
(1.93)
3
1314
u. probosc&&a
-0.33
1.37
5
14-15
U. proboscideo
-0.15
1.33
4
IS16
U. proboscidea
-0.26
1.44
2
(continued)
1625
Ecology and isotopic composition of foraminifera Table 3. sllhl Interval
Species
Continued
sea 613C
South China Sea #*O
Numberof
Interval
Specimens
613C
g’s0
Number of
Specimens
10
Con O-1
C. bradyi
(-0.08)
(1.22)
5
l-l .5
C. bradyi
-0.32
1.11
4
1.5-Z
C. bradyi
-0.14
I .24
3
2-2.5
C. bradyi
-0.04
1.23
3
o-1
c. wwllers10rfi
0.19
0.96
3
O-l
G. broeckhiaw
-1.09
I .46
2
&I
0. umbonorru
-1.28
1.4
4
0. umbonarus
-1.19
1.39
4
(-0.03)
(1.1)
3
-0.76
1.13
2
1.5-2 core
Species
20
O-l
C. bradyi
O-1
C. robertsonionur
0-I
0. !mlbomzur
(-0.59)
(1.44)
2
I .5-z
0. umbonorw
-0.65
1.31
2
3.5-4.5
0. umbonatw
-0.77
I .32
3
0. umbonatur
(-1.4)
(I .53)
3
2-2.5
V. mexicana
(-0.72)
(1.1)
17
2.5-3
V. mexicana
(-0.76)
(1.12)
22
Core 16 &I core
18
South China Sea Core 3 (1095 m) >150 pm (#/Socc) Clblddddfs bradyi
Ceratobnhntnn pdfka
Fig. 3. Vertical profiles of selected species from the > 150 pm fraction of core 3 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 data from subcores 3-1 and 3-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
1626
A. E. Rathbum et al.
South China Sea Core 4 (2150 m) ~450 pm (W&c) OrbbmaUs umbmatua 0 0
5
10
paclfka
centobulbnbu
15
r-0
Organic
0.0
03
15
10
I
Carbon
0.4
0.6
4.
0.8
Fig. 4. Vertical profiles of selected species from the > 150 pm fraction of core 4 (no. per 50 cm’) plotted vs sediment depth (cm). Fauna1 data from subcores 4-l and 4-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
Agglutinated foraminifera dominate the > 150 pm fraction of the South China Sea subcores and reach maximum densities in the top 1 cm in subcores from the 1095 m site (core 3) in one subcore from the 2150 m site (subcore 4-l), and in one subcore from 2950 m (core 2-l). The remainder of the subcores examined show density maxima of the agglutinate assemblages below the upper 1 cm. Graphs and data tables of total agglutinated assemblages are included elsewhere (Tappa, 1992). The presence of relatively large numbers of stained specimens deep in the sediments in core 3 is similar to patterns seen from water depths of 1200 m or less in other regions (Loubere and Gary, 1990; Corliss and van Weering, 1993). Since micro-scale gradients in oxygen (Meyers et al., 1987, 1988; Langer et al., 1989; Thomsen and Altenbach, 1993) and increases in organic carbon contents near macrofaunal burrows (Aller and Aller, 1986) have been shown to influence meiofaunal abundances and distributions, subsurface fauna1 patterns in core 3 are interpreted to result from suitable deep infaunal habitats created by macrofaunal burrowing. Laboratory X-radiographs showed evidence for extensive bioturbation throughout the length of core 3 sediments. Fauna1 abundances of the > 150 urn fraction in core 2 are relatively low, and based on a qualitative examination of the 63-l 50 l,trn fraction of surficial sediments of this core, the smaller size fraction also does not contain high fauna1 abundances. In contrast to the relatively diverse assemblage in core 3 (1095m), core 1 (3980m) is characterized by a low-diversity, infaunal assemblage dominated by Chilostomella oolina. The absence of a stained epifaunal assemblage, combined with the presence of abundant, living infauna in core 1, indicate that this assemblage represents a living population, and does not result from enhanced preservation due to rapid burial. The increase in C. oolina
1627
Ecology and isotopic composition of foraminifera
south china sea Core 2 (2950 m) >150 pm (#/gocc)
Of
01
0.4
0s
0.6
0
30
so
90
no
0
5
$
1
F
15
IO
~
Fig. 5. Vertical profiles of total calcareous taxa and total foraminifera from the > 150 pm fraction of core 2 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 dam from subcores 2-1 and 2-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
South China Sea Core 1 (39gom) >150 pm (#lsocc)
0-k
Cubm
%
Fig. 6. Vertical profiles of total calcareous taxa and total foraminifera from the > 150 urn fraction of core 1 (no. per 50 cm3) plotted vs sediment depth (cm). Fauna1 data from subcores l-l and l-2 combined and plotted as an average are connected with a line, and data from each subcore are plotted as a vertical bar. Organic carbon weight percentages and pore-water oxygen levels within the sediments are also plotted.
1628
A. E. Rathbumet al.
densities at 6-8 cm in this core coincides with an increase in agglutinate densities (which also have an infaunal density maximum) and a sharp increase in organic carbon contents (Fig. 6). The X-radiograph of the reference subcore shows evidence for bioturbation throughout the core, with no observable turbidite features. The significant increase in subsurface organic carbon contents, together with unusually high organic carbon contents at this water depth, however, are consistent with the occurrence of turbiditic sedimentation. Calvert et al. (1993) note that 8t3C,rsanic values of the surficial sediments of both the Sulu and South China Sea basins do not decrease uniformly with increasing water depth, suggesting that there is organic matter input from shallow-water or terrestrial sources to deep water environments. There is no hydrological evidence for a localized region of high productivity in this area of the South China Sea, and the relatively high organic carbon values probably result from the transport of organic-rich sediments from shallower depths via turbidites; bioturbation has obscured many of the laminations characteristic of turbidites. Pore-water oxygen levels were not measured in this box core, but the pore-water Mn profile suggests that pore-water oxygen values reach zero between 8 cm and 10 cm (Fig. 6). Box core 1 has the highest apparent mixing coefficient of the box cores examined by Fuglseth (1991), at about 1.5 cm* year- ‘. Sulu Sea fauna
Detailed fauna1 and geochemical results of Sulu Sea cores are given in Rathbum and Corliss (1994), and microhabitat preferences of dominant taxa are given in Table 2. Vertical distribution patterns of abundant species used in isotope analyses are shown in Figs 7-10. Fauna1 data from other cores are presented but are not illustrated. Oxic pore-water penetration depths and surficial organic carbon values for Sulu Sea cores are plotted in Fig. Il. Only a few brief comments regarding cores 8 (1005 m) and 18 (45 15 m) are given below. Rathburn and Corliss (1994) attributed the occurrence of relatively large densities of stained benthic foraminfera at 13-16 cm in core 8 (1005 m) to a rapid burial event which preserved an epifaunal assemblage by preventing significant degradation of protoplasm. Recolonization of the surficial sediments and preservation of the buried organic material (including protoplasm) would produce the observed fauna1 patterns (Fig. 8). The occurrence of a rapid burial event is also supported by laboratory X-radiographs, sedimentation rates and subsurface organic carbon patterns (Rathburn and Corliss, 1994). Although turbidite sedimentation is evident in core 18 (4515), Rathbum and Corliss (1994) have noted that the fauna1 patterns are not consistent with a rapidly buried assemblage, but instead indicate that stained specimens represent the living population (Fig. 10). The calcareous assemblage of core 18 (4515 m) consists of over 14 species found primarily below 1.5 cm. The > 150 urn and > 63 urn fractions are dominated by Vulvulineriu mexicana, which has a maximum in the 2.5-3 cm interval (Fig. 10). Maximum abundances of Globobulimina sp. 2 are found between 8 and 10 cm, while specimens of Chilostomella occur between 5 and 11 cm. Organic carbon contents are significantly higher in core 18 compared to values obtained from the 3000 and 4000 m cores (Figs 10 and 11) and show a significant maximum (-0.9-l .5%) at 8-l 1 cm (Fig. 10). Onboard X-radiograph analysis and 14C profile data indicate that turbidite sedimentation influenced box core 18. The relatively high organic carbon values at this depth coupled with the sharp subsurface maxima in organic carbon are also consistent with the suggestion that turbiditic sedimentation occurred.
1629
Ecology and isotopic composition of foraminifera
Sulu Sea Core 12(510m) >150pl (#/5occ) Clbkldddes 0
pacby&rms LO
5
Bollmloa IS
Uvigerbw
mukans
5
to
I5
0
pcregrlna
s
LO
15
*I+-Clbkldolda
0
5
nvelkrstwfl
to
15
20
I
Fig. 7. Vertical profiles of selected species from subcore 12-2 (no. per 50 cn?; > 150 pm fraction) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with symbols in Fig. 12.
Sulu Sea Core 8 (1005 m) >150 pm (#/SOcc) Anomallnddar 0
5
Clbkldokka
cdll~en
16
IS
Uvlgerlna 20
pachyderma
0
to
SIphonIns
0rldorpslls
pmbosdda 20
rrtkulnta
30
0
5
umbonatus 10
Melonis
IS
Chllostomelk 20
0
s
10
oollns IS
Pmnls
Fig. 8. Vertical profiles of selected species from subcore 8-l (no. per 5Ocm’; > 150 urn fraction) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with symbols in Fig. 13. Hatched areas mark buried top interval.
20
1630
A. E. Rathbum et al.
Sulu Sea
Core 10W80
m)
>lSO pm W*C)
(a) Clbkldoldeo dkrstdl
Clblddotdes
Gymtdlnotda
bradyi
brocdtbtana
L-2 , 0
10
Sulu Sea Core 2OW@m) >lSO pm WOcc)
(b) Ctbtctdddrr 0
5
Ortdor~alts umlmaatus
bradyl to
Clbkldoidrs
0
15
mberkonlsnus 5
10
IS
Fig. 9. (a) Vertical profiles of selected species from the > 150 pm fraction of subcore 10-2 (no. per 50cm3) plotted vs sediment depth (cm). (b) Vertical profiles of selected taxa from the > 150 urn fraction of subcore 20-2 (no. per 50cm3) plotted vs sediment depth (cm). These taxa were also analysed for stable isotope compositions and the symbols used for each taxon correspond with
Sulu Sea Core 18 4515 m (#/xkc) >150 pm
Fig. 10. Vertical profiles of selected species (no. per 50 cm’) from the > 150 )rm fractions of subcore 18-2 plotted vs sediment depth (cm); organic carbon and pore-water oxygen contents are also plotted.
Ecology and isotopic composition of foraminifera Pore-Water Oxygen Penetration Depth (cm) 10
5
0
0
15
1631
Surfidal Organic Carbon 96 20
ib
0.4 0.5 0.6 0.7 0.8 0.9 1.0
1000
F
Fig. 11. Oxic pore-water penetration depth (cm) and surficial organic carbon (weight %) for each Sulu Sea core plotted vs sediment depth (cm).
Sulu Sea stable isotope analyses
The 613C and 6r80 values of abundant taxa are given in Table 3. Samples which yielded isotope values with a standard deviation of > 0.05 are shown in parentheses and are not included in the figure plots or discussed in the text. The isotopic composition of specimens from cores 15, 16, and 18 were not determined because of low numbers of specimens, and core 9 specimens were not analyzed for isotopes because core 9 was taken at the same site as core 10. Analyses of X-ray diffraction data showed that Bolivinopsis cubensis has a calcitic test, while the test of Gavelinopsis lobatulus is aragonitic. The other aragonitic taxa included in the isotope analyses are Ceratobulimina pacljica and H. elegans. The distribution of carbon and oxygen isotope data for each taxon in Sulu Sea cores is presented in Figs 12 and 13, while Fig. 14 illustrates the distribution of stable isotope data from core 3 (1095 m) in the South China Sea. The average oxygen isotope differences (A6180) between test 6180 and the calculated at80 of equilibrium calcite (8’80,.c.), and the average carbon isotope differences (A613C) between estimated bottom-water 613C (6’3Ct,,.) and test 613C for each taxon with more than one isotope analysis are presented in Fig. 15. For the purpose of comparison, the 8180 (PDB) of calcite in equilibrium with water (6180,,c,, PDBj) of a given 6180 SMOW composition (8’80((b. w,. SMOW))and temperature T (in degrees Kelvin) was calculated using the following equations (provided by D. McCorkle, personal communication, 1995): J’80+.,~~~~
=
Ie
x ~180 ((2.78xlo'/T2)-(2.89/10')) (b.w.,SMOW) + 1000)) - 1000
6180(,,.,poaj = (0.97006 x S’80~,.,.,s~ow$ - 29.94
(1)
(2)
Equation (1) is based on the temperature relationship given in equation (3) from Friedman and O’Neil(1977), and differs slightly from the equations given in McCorkle et al. (1990) that are based on equations from O’Neil et al. (1969). 10’ln cr(CaCOs - H20) = 2.78 x lo/T2 - 2.89.
(3)
We estimated bottom-water 8180 (6’80t,w.) to be - 0.1% SMOW for each site (based on western Pacific Water intermediate- and deep-water values). Without bottom- or surficial pore-water 613C data, it is difficult to accurately estimate the 6r3C of equilibrium calcite (Sr3C,.,.) in the Sulu and South China Seas. Northern Pacific
A. E. Rathbum et al.
1632
Sulu
sea PO (4&d
613C (%I
Core 12 (510 m)
~
,jyk$y
B
y&L
j-
j_L+z
Core 10 (1980 m)
m Astmnonbn novomahdknm
~~~~~~~
~~~~
~~~~~n~l ?? CibWdcddeabndyl
Fig. 12. The gL3Cand 6rsO values (%o)for significant species from subcores 12-2, 10-2, and 20-2 are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (6) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each species are also indicated. Because of the number of data points, the data have been separated into four plots.
Ocean GEOSECS stations 222,224,226,229,235,241,246, and 251 include bottom-water F13Cvalues from appropriate depths (near 400 m, for Sulu Sea estimates, and 1000 m down to N 2000 m for South China Sea estimates), but even using the correction factors suggested by Kroopnick (1985), the data are variable. As noted by McCorkle and Keigwin (1994), GEOSECS 613C data from many of the western Pacific sites are equivocal, especially those from the upper 1000 m of the water column, making it difficult to assess the 613Ccomposition of water moving into the South China and Sulu Sea Basins. For this reason, we have chosen to estimate the 6r3C value of bottom waters in the Sulu and South China Seas based on the relationship between apparent oxygen utilization (AOU) and 613C given in Kroopnick (1985). Using the relationship between AOU (AOU = (dissolved oxygen at saturation) (measured dissolved oxygen levels)) and 613C as presented in Kroopnick (1985) (equation (4)) and the solubility of oxygen at measured temperatures and salinities given in Weiss (1970), 613C values were calculated for bottom-waters in the South China and Sulu Seas. 613C = 1.5 - 0.0075 x AOU
(4)
Ecology and isotopic composition of foraminifera
Sulu
8
sea
Core (1005 m)
(%cPDW PO
Fig. 13. The 6t3C and 6’*0 values (%) for significant species from subcore 8-l are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (8) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each taxon are also indicated. Some deep infaunal occurrences are due to turbidite burial of an epifaunal assemblage (see text for discussion).
South China Sea Core 3 (1095 m) (52~PDW
Fig. 14. The 8r3C and 6’*0 values (?&I)for significant species from subcore 3-2 are plotted vs sediment depth (cm). Stable isotope values are plotted in standard delta (8) notation relative to the Peedee Belemnite (PDB) standard. The microhabitat preferences of each taxon are also indicated.
1633
1634
A. E. Rathbum et al. Average Stable Isotope differences
sea
suhl
SouthChina Sea A S’“0
A S’*O -1
0
1
-2
2
-4
-1
0
1
.
.
A 6°C -1
0
1
A
0
-2
6°C 0
2
spp.
(E) Clbkklokka Clbkklddes bdyl
6) DW
pro*
(Tl &Gddddw bndyl 0 Mekloak amoh 0 Drldmnlk umbonntm (S) Url&ns Prdmncidu (8 Bulimha medana
Fig. 15. Average values for the difference between test gL80 values and equilibrium calcite 6’*0 (AS’*O), and for the difference between test 6% values and ambient bottom-water 613C(AS”C), for each taxon represented by more than a single isotope analysis. The 6’*0 for equilibrium calcite for the bottom-water (S’sO,,) at each site was calculated as described in the text, and subtracted from the g’s0 values for specimens analysed from each core. The 6% values of each taxon represented by more than a single isotope analysis was subtracted from the estimated bottom-water 613C(6’3C b,w.) at each site. The average isotopic difference for each taxon was computed and plotted along with the standard deviation. As plotted, g’sO,.,. and 8’3Cb.W.=O. Note that the unusual 6”O and 613Cvalues of -0.71% and - l.O%, respectively, for S. reticuluta at 0-l cm in core 8 were not included in the average or standard deviation calculations (see Table 3 and Fig. 15). Species labeled with an asterisk, *, have an aragonitic test. Microhabitat preferences are delineated by the following symbols: E, epifaunal; T, transitional; S, shallow infaunal; D, deep infaunal.
These calculated values (Table 1) are within the expected range of 613C values based on GEOSECS 613C data and the results reported by McCorkle and Keigwin (1994). We believe that our estimates are correct to within 0.2%0.Despite slightly higher dissolved oxygen levels in the South China Sea, bottom-water 613C values are more negative than those of the Sulu Sea because of the differences in water temperature and oxygen solubility (and AOU) of the bottom-waters of these basins. The differences between bottom-water 613C estimates and the measured 613C values of benthic foraminiferal specimens at each site are calculated and reported as A6r3C values. Average A6r3C and A6r8O values for each South China Sea and Sulu Sea taxon which is represented by more than one stable isotope analysis are presented in Fig. 15.
Standing stocks Results from this study yield standing stocks from 2982 to 66150 cm2 in the Sulu Sea and 2967 to 239150 cm2 in the South China Sea, and are within the range of values reported for other regions (Table 1). Total foraminiferal standing stocks are relatively high in the shallower sites in both basins and generally decrease with increasing water depth. The
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variability between the 4000 m cores in the Sulu Sea (15 and 16) is probably due to the heterogeneous distribution of siliceous sponge skeletal material (Rathbum and Corliss, 1994). Standing stocks of the calcareous assemblage, which is more representative of the fossil assemblage due to the post-mortem destruction of most agglutinated taxa, also generally decrease with increasing water depth to the deepest site, where standing stocks increase again. The data for core 8 are not considered reliable for standing stocks because of the influence of preserved specimens buried deep within the sediments. While other environmental variables remain relatively uniform in both basins, organic carbon in the sediments generally decreases with increasing water depth, then increases dramatically at the deep sites (Figs 2 and 11). This increase is due to organic carbon transported from shallower regions by turbidites and corresponds to increases in infaunal taxa and subsurface accumulation of organic carbon (Figs 6 and 10). Comparisons of standing stocks reported in other studies are often difficult because of the different size fractions used or because infaunal populations were not sampled. DISCUSSION Generalfaunal characteristics: South China Sea
Agglutinated assemblages dominate the cores and account for a significant portion of the total foraminiferal assemblage. Calcareous assemblages reach maximum densities in the top 1 cm of sediments in both subcores from box cores 3 and 4, while box cores 1 and 2 yielded subsurface density maxima of calcareous assemblages. Densities and diversities decrease with increasing water depth down to 3000 m, below which diversity remains relatively uniform. Densities increase significantly in the 4000 m core due to the additional organic carbon available at the deepest site (Table 1) (the relationship between fauna and organic carbon is discussed below). In the South China Sea, G. lobatulus, Uvigerina species, C. bradyi, C. pacifica, B. cubensis, C. oolina, H. elegans, and 0. culter are common in subcores from 1095 m (core 3), and 0. culter, C. pacljica, Astrononion sp, 0. umbonatus and P. subcarinata are common species in subcores 4-l and 4-2 from 2150 m (Fig. 2). Very few foraminifera are observed in subcores from the 2950m site (core 2), and Cibicidoiaks, Gyroidinoides and Oridorsalis are represented. Subcores from the deepest site (l-l and l-2) are characterized by infaunal populations of C. oolina (Fig. 2). Comparisons with Sulu Sea
The distribution patterns and densities of Sulu Sea species are similar to those in the South China Sea. Agglutinated taxa dominate Sulu Sea cores as they do in the South China Sea sediments, with both calcareous and agglutinate assemblages typically reaching maximum densities in the top 1 cm. Diversity and abundances generally decrease with increasing depth in the sediment and increasing water depth in both basins. In the Sulu Sea Basin, diversity in the deepest core (4515 m) is similar to that in the 4000 m cores, and is probably affected by the greater availability of organic carbon deposited by turbidites; a similar pattern is observed between the 4000 m and the 3000 m sites in the South China Sea (Table 1). In the Sulu Sea, Cibicidoides and Uvigerina are the dominant genera (> 10% of the calcareous assemblage) at 5 10 m (core 12) and together with Siphonina, are also dominant
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taxa at 1005 m (core 8). Dominant genera at 2000 m (cores 9 and 10) include Gyroidinoides, Oridorsalis, Cibicidoides and, in one core, milioline taxa. The 3000 and 4000 m cores are dominated by C. bradyi and 0. umbonatus, while the most abundant taxon in the deepest core (45 15 m) is the infaunal V. mexicana. The infaunal pattern of V. mexicana is similar to the fauna1 pattern of C. oolina observed in the deepest core of the South China Sea in that both sites are below the lysocline and are interpreted to have been influenced by turbidite sedimentation, with organic carbon brought in from shallower environments. Although differences in dominant taxa exist between basins, the general characteristics of the fauna1 patterns are remarkably similar. Microhabitat preferences
Microhabitat preferences of Sulu and South China Sea taxa have been identified based on vertical distribution patterns and interpretations reported in Rathburn and Corliss (1994) and Tappa (1992) and are summarized in Table 2. In addition to the distribution patterns noted by Corliss (1985, 1991) taxa such as C. bradyi and 0. umbonatus have transitional distributions and are found living from 0 to N 4 cm in the sediments. Taxa which are found in both the Sulu and South China Seas show similar distribution patterns and include C. bradyi, U. proboscidea, H. elegans, and C. oolina. Results from this study support suggestions by Rathbum and Corliss (1994) that Chilostomella is adapted to take advantage of subsurface accumulations of labile organic carbon, even in deep turbiditic sediments near the CCD. South China Sea species which are not common in the Sulu Sea include: the transitional taxa, G. lobatulus and 0. culter, which have maxima at the surface with significant occurrences deeper in the sediments; C. pacz$ca, which has a shallow infaunal maximum from 0-2cm; and B. cubensis, with maximum abundances in deep infaunal (> 4 cm) habitats (Fig. 3). It should be noted, however, that many of the South China Sea taxa, such as B. cubensis, G. lobatulus, and 0. culter, are found primarily in core 3, which may be significantly affected by bioturbation. The morphologies of most taxa are related to their microhabitats, as discussed by Corliss (1985,1991), Corliss and Chen (1988), and RathbumandCorliss (1994). Theplanoconvex to biconvex morphologies of G. lobatulus and 0. culter, however, are considered epifaunal attributes(Corliss, 1985,1991;CorlissandChen, 1988),butthesetaxaarealsofoundwithinthe sediments in core 3. Large numbers of epifaunal taxa occur in the 13-14 cm interval in Sulu Sea core 8, and Rathburn and Corliss (1994) interpreted this occurrence as a preserved epifaunal assemblage that was buried by turbiditic sedimentation. No buried epifaunal assemblage was observed in core 3. Occurrences of stained fauna deep within bioturbated sediments, however, is consistent with observations in the Skagerrak, where Corliss and van Weering (1993) reported complex distribution patterns of benthic foraminifera in bioturbated, organic-rich sediments. These infaunal patterns were attributed to heterogeneity in subsurface environments due to a relatively high amount of biological activity. Variables influencing fauna1 patterns
Environmental variables such as temperature (e.g. Polski, 1959; Phleger, 1960; Biswas, 1976), organic carbon (e.g. Lutze, 1980; Miller and Lohmann, 1982; Lutze and Coulboum, 1984; Corliss and Chen, 1988; Caralp, 1989; Corliss and Emerson, 1990; Herguera and Berger, 1991) and bottom-water oxygen (e.g. Lohmann, 1978; Schnitker, 1979; Burke, 1981;
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Perez-Cruz and Machain-Castillo, 1990; Kaiho, 1991, 1994) have been suggested to significantly influence some species of benthic foraminifera. The relatively uniform bottom-water oxygen and temperature conditions within the Sulu and South China Seas combined with the contrasting bottom-water properties of these basins make this an excellent area in which to compare fauna1 assemblages and examine the variables which influence benthic foraminiferal distribution patterns. Temperature
Significant differences exist in dominant taxa (2 > 10% of calcareous fauna) in the > 150 pm fraction between the thermospheric Sulu Sea Basin and the psychrospheric South China Sea basin as shown in Fig. 2. Gavelinopsis, Bolivinopsis, Astrononion, Osangularia, and Ceratobulimina are common taxa in the South China Sea but are rare to absent in Sulu Sea sediments. Siphonina and Valvulineria are dominant taxa at certain depths in the Sulu Sea, but are absent in South China Sea samples. Since other environmental variables are similar between basins, these differences in dominant taxa are suggested to result from the large differences in bottom-water temperatures. Differences in selective predation, specific food requirements, and recruitment may also influence fauna1 distributions, but the proximity of the basins indicates that these factors are not primary controls of the observed patterns. Although fauna1 changes are evident within each basin, temperature does not vary significantly below 1000 m within the Sulu Sea and South China Sea basins (Table l), suggesting that bottom-water temperature cannot account for the fauna1 changes observed within each basin. The evidence for the influence of temperature as a controlling factor is limited, as the South China Sea data is based primarily on one core 3, and differences occur between sites within each basin. Nevertheless, the large difference in temperature between the basins seem to influence the distribution of some taxa. Bottom-water oxygen
Although dissolved bottom-water oxygen content has been ascribed as a primary factor controlling some species of benthic foraminifera (e.g. Lohmann, 1978; Burke, 1981; PerezCruz and Machain-Castillo, 1990), results from this study do not support this assertion. Many of these species which have been suggested to be associated with low-oxygen conditions, such as Bolivina and Bulimina, are present in the shallow sites of the Sulu Sea but do not occur in significant numbers in deeper water despite the similarity of bottom-water oxygen levels (Rathburn and Corliss, 1994). Comparisons of living assemblage distributions with core-top dead assemblages indicate that the absences of these “low-oxygen taxa” are not due to seasonal variations or recent flushing of the Sulu Basin (Rathbum and Miao, 1995). In the South China Sea, bottom-water oxygen levels are also quite low (up to about 1.8 ml l-l), and only slightly higher than those of the Sulu Sea sites, increasing by > 0.5 ml 1-l from 1000 m to 4000 m (Fig. 2). The > 150 pm fraction data and a qualitative examination of the 63-150 l.un fraction in South China Sea samples do not reveal high numbers of “low oxygen taxa” such as Bolivina and Bulimina. Organic carbon
Organic carbon has been suggested to be an important influence on the abundances and distribution patterns of deep-sea benthic foraminifera, including those in the Sulu Sea (Rathburn and Corliss, 1994). The South China Sea data are consistent with these observations, although it is difficult to assess the distributions of smaller taxa, such as
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Bolivina, without quantitative data on the 63-150 pm fraction. Taxa such as Uvigerina, Bulimina, Bolivina, and Chilostomella, which have been associated with high organic carbon
environments in the Sulu Sea (Rathburn and Corliss, 1994), have similar distributions in the South China Sea. Uvigerina, Bulimina, and Bolivina are most abundant in the shallowest cores (510 and 1005 m: Sulu Sea; 1095 m: South China Sea), but are not abundant in deeper sites where organic carbon values are lower. In contrast to living (this study) and fossil data from samples off the northwestern coast of Palawan, fossil material from the surficial sediments of gravity cores taken in the South China Sea off the southwestern coast of Palawan yielded significant percentages of Bolivina and Bulimina (Miao and Thunell, 1993). Since the bottom-water properties (oxygen content, temperature, and salinity) of the southwestern South China Sea are similar to those of our South China Sea study area, but organic carbon values of the sediments are significantly higher (0.84-2.22%), occurrences of these taxa appear to be related to the presence of organic carbon in the sediments in the South China Sea as well as the Sulu Sea. The infaunal species, Chilostomella oolina, is abundant in sediments from 1095 and 3980 m in the South China sea and 510, 1005 and 4515 m in the Sulu Sea where subsurface organic carbon levels are higher (> 0.74%) (Figs 3 and 11). The relatively high organic carbon contents found in the deepest core from each basin are interpreted to result from turbiditic sedimentation. The occurrence of high-abundance, low-diversity assemblages dominated by C. oolina in the deepest core of the South China Sea is consistent with the idea that Chilostomella is able to take advantage of subsurface accumulations of organic carbon in abyssal turbiditic sediments. Although surficial organic carbon levels are higher in the deepest sites than at shallower depths of both basins, surficial sediments in the deepest cores (South China Sea core 1: 3980m and Sulu Sea core 18: 4515m) are inhabited almost exclusively by agglutinated taxa. The corrosivity of bottom waters (CCD is 3800-4000 m in the South China Sea; 45004800 m in the Sulu Sea) may prevent many calcareous taxa from inhabiting the top 2-5 cm of sediments in deeper portions of these basins. Calcareous species that prevail under these conditions are those which are adapted to the low-oxygen environments deeper in the sediments where labile organic carbon is available. These deep-dwelling specimens can be preserved in the geologic record of these areas (see Resig, 1981 and Miao, 1993) and more work is needed on these environments. Standing stock
Total foraminiferal standing stocks generally decrease with increasing water depth, although standing stocks for calcareous taxa increase in the deepest cores of both basins (Table 1). Previous studies have reported wide ranges in the standing stocks of deep-sea foraminifera (e.g. Coull et al., 1977; Thiel, 1979, 1983; Snider et al., 1984; Gooday, 1986; Alongi, 1987; Mackensen and Douglas, 1989; Silva et al., 1996). Comparisons between studies are often difficult because of the different methodologies and sieve sizes used, but Gooday (1986) noted that deep-sea foraminiferal standing stocks are typically reported as being lower than 1000 per 50 cm2. Except for the three shallowest sites (cores 12,8, and 3), all of the cores in the study area fall below 1000 specimens per 50 cm2 in the > 150 pm size fraction (Table 1). When the 63-150 pm fraction is also included, however, cores 9, 10 and 20 yield densities close to 1000 specimens per 50 cm2. In this study, higher organic carbon contents generally yield higher standing stocks within a given basin, but increases in standing stocks are not necessarily proportional to the
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corresponding increase in organic carbon. There is a general relationship between relative suticial organic carbon contents and fauna1 abundances within a basin, but the number of specimens per milligram organic carbon ratio is not consistent between basins. A number of studies have suggested that deep-sea macrofaunal and meiofaunal standing stocks are directly related to food availability (see Thiel, 1983 and Jumars and Wheatcroft, 1989 for reviews). Previous workers have noted, however, that organic carbon contents of deep-sea sediments correlate only approximately with biomass values and that better correlations are obtained with parameters more closely related to primary productivity such as chlorophyll (Pfannkuche and Thiel, 1987; Altenbach and Sarnthein, 1989) and phytodetrital flux (Gooday, 1988; Gooday and Lambshead, 1989; Altenbach, 1992). Different components of organic carbon may provide direct (Caralp, 1989; Delaca, 1982; Delaca et al., 1980,198 1) or indirect food sources (Langer and Gehring, 1993; Goldstein and Corliss, 1994) for different foraminiferal species, and some varieties of organic carbon may not be available as food sources for foraminifera. The correlations between fauna1 patterns and surficial and turbiditic subsurface organic carbon values in this study indicate that there are differences in the quality of organic carbon as a food source for benthic foraminifera, as suggested by other workers (Caralp, 1989; Altenbach and Sarnthein, 1989; Gooday and Turley, 1990; Gooday et al., 1992; Rathbum and Corliss, 1994). The lack of a direct relationship between population densities and organic carbon values in this study also indicates that other factors such as the quality of organic carbon influence foraminiferal standing stocks (e.g. Lipps, 1983; Gooday and Turley, 1990). Stable isotope compositions Carbon isotopes
The 613C data generally support the suggestion that the carbon isotopic composition of benthic foraminifera is influenced by microhabitat preferences. In typical deep-sea sediments, pore-water 613C decreases down core as a result of the oxidation of organic matter rich in I2C (McCorkle et al., 1985, 1990; Sackett, 1989). The 613C pore-water gradient is reflected in the carbon isotopic composition of taxa living on and within the sediments; epifaunal species have the highest values and are closest to equilibrium with the overlying bottom-waters, while infaunal taxa have lower 613C values which are related to the isotopic values of pore-waters (McCorkle et al., 1990). In this study, epifaunal taxa such as C. wuellerstorji, C. pachyderma, and Cibicidoides spp. typically have the highest 613C, deep infaunal species such as C. oolina have the lowest values, and transitional and shallow infaunal taxa such as G. subglobosa, U. probosidea, and B. mexicana have intermediate values (Figs 12-15). These data are consistent with the idea that microhabitat preferences influence the carbon isotopic composition of individual species. Vital effects are indicated, however, for the deep infaunal species, B. cubensis, whose 613C values are not consistent with those of other taxa with similar microhabitat preferences. Although infaunal species typically have lower 613C than epifaunal taxa, B. cubensis has significantly higher carbon isotope values than the epifaunal Cibicidoides spp. Bolivinopsis cubensis constructs a test which is granular in appearance, and the microstructure of the shell material may influence the isotopic values of the test. The differences in isotopic values between B. cubensis and the other taxa in core 3 may reflect interspecific biological differences in fractionating isotopes for shell construction, or may be related to other
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differences between species, such as food preferences. The relationship between the ecological preferences and isotopic compositions of B. cubensis is difficult to assess because this species was abundant in only one core. To our knowledge, this study provides the only isotopic data from representatives of this species. The two aragonitic species in this core also do not conform to the pattern seen in calcitic species. Gavelinopsis lobatulus has a transitional microhabitat preference, but has lower 613C values than deep infaunal taxa in core 3, whereas the shallow infaunal species, C. pac$ca, has significantly higher carbon isotope values than the epifaunal Cibicidoides spp. Grossman (1984a,b, 1987) and Grossman and Ku (1986) observed that the 613C values of aragonitic tests can be influenced by bottom-water temperatures, while no such effects were suggested for the 613C of calcitic taxa. Temperature effects may influence the 613C values of G. lobatulus and C. pacljica but cannot account for the large differences between these species. Note that H. elegans yields carbon isotope values that conform to the pattern of relatively high 613C for epifaunal taxa, but which are also consistent with the relatively high values reported for this aragonitic species by previous authors (e.g. Grossman and Ku, 1986; McCorkle et al., 1990). Plots of average A613C values for each taxon represented by multiple stable isotope analyses show patterns similar to those observed by McCorkle et al. (1990) (Fig. 15). Epifaunal taxa such as C. pachyderma and Cibicidoides spp. tend to have higher A613C values relative to transitional and shallow infaunal species, with a range of about 2%0.The deep infaunal C. oolina has a low A613C value compared to epifauna, shallow infauna and transitional species, but is only about 2% lighter than equilibrium calcite as compared with the - 4% A613C values of Chilostomella reported by McCorkle et al. (1990). The aragonitic species, H. elegans and C. pacifica, have high A613C values as expected, but the aragonitic taxon, G. lobatulus, has an unexpectedly low A613C value, and the deep infaunal species, B. cubensis, has an unexpectedly high Ac1613C value for a calcitic species. Previous studies report 613C values of 0. umbonatus as significantly lower and more variable than those of C. wuellerstor- (Woodruff et al., 1980; Belanger et al., 1981; Graham et al., 1981; Berger and Wefer, 1988). The transitional infaunal (0-4cm) microhabitat preference of 0. umbonatus documented in the Sulu Sea cores (Rathburn and Corliss, 1994) is reflected in lower A613C values (Figs 12-15, Table 3), which can account for the “anomalous” isotopic values noted in previous studies. This study did not find high variability in the A13C values of 0. umbonatus, but the eurytopic lifestyle of this species could also account for variability in carbon isotopic composition. Carbon isotopes of taxa found in the same interval
The range in 613C for specimens from the same interval within a core may be substantial (about -l&1.6% in core 12; -3.&0.3°h for core 8; - 1.3~.2s/oo for core 10; and -0.80.0%0for core 20), but within these intervals taxa identified as epifaunal from this and other studies have higher 613C than infaunal taxa (Fig. 12). Except for 0. umbonatus in core 20 and U. peregrina in core 3, most taxa found over a depth range within the sediments do not show consistent gradients in 613C as would be expected if carbon isotopic compositions were influenced only by the average pore-water environments where they were found. Differences in isotopic compositions between living (stained) benthic foraminifera taken from the same interval as seen in this study and in previous studies (Woodruff et al., 1980; Grossman, 1984a, b; McCorkle et al., 1990; Loubere et al., 1995) can be explained by: (i)
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vertical movement of infaunal taxa within the sediments, with species secreting all or portions of the test in deeper sediments; (ii) differences in food preferences; (iii) vertical mixing of specimens by bioturbation; (iv) vital effects (differences in isotopic fractionation due to inherent biological processes); (v) microenvironments within the 1 cm sample interval; or some combination of these explanations. These explanations also have to account for both the consistency of 613C compositions of taxa within the sediments and observed distribution patterns. Seasonal vertical movements of some deep-sea benthic foraminifera have been reported in the northeastern Atlantic (Gooday, 1988) and the Adriatic Sea (Jorissen et al., 1992), but not in the California borderlands (Silva et al., 1996). Given that burrowing is the most energy-consuming mode of movement (Jumars and Wheatcroft, 1989) it would be highly inefficient to consume food near the surface (such as in core 12) and burrow deeper to secrete CaC03. This is especially true in environments like the deep-sea, where food availability may be periodic and where opportunistic behavior may prevail. Ontogenetic changes in sediment-depth preferences are possible, but fauna1 results from different size fractions in the Sulu Sea suggest that this is not likely (Rathburn and Corliss, 1994). Food partitioning has been reported in other meiofaunal populations (Carman and Thistle, 1985), and since food sources can affect the carbon isotopic signals of organisms (Sackett, 1989; Wefer and Berger, 1991) it is possible that food preferences may contribute to differences in isotopic compositions of foraminiferal species found in the same interval. Food preferences are likely to be related to microhabitat preferences and could also account for the consistency of isotopic compositions of each species over a range of depths within the sediment. In addition to the possibility of a direct influence of food on foraminiferal shell chemistry, differences in food preferences could be an indirect influence by causing species to congregate near micro-food sources; similar organic food sources might generate similar pore-water microenvironments (see discussion below). The effects of food preferences on the isotopic compositions of benthic foraminifera, however, have not been examined. Mixing by macrofaunal bioturbation may vertically transport individuals in the sediment. The mixing of foraminifera from different sediment depths by bioturbation could account for the consistency of isotopic signals within a taxon and for the interspecific isotopic differences between specimens from the same interval. Bioturbation, however, cannot account for the distribution patterns of benthic foraminifera within the sediments (e.g. Corliss and Emerson, 1990). McCorkle et al. (1990) show that the carbon isotopic compositions of benthic foraminifera are significantly influenced by the microenvironments where they live. Bioturbated individuals may stop growing after being transported to a marginal habitat, and the 613C composition of their tests should, in part, reflect the microhabitat in which they prefer living (where their tests were secreted). Although a few individuals may live in marginal microhabitats to which they have been transported, the occurrence of significant numbers of specimens within the sediments examined suggests that these sediment intervals are within the microhabitat range of the taxa represented. If these taxa are living within their optimal microhabitat range, mixing may account for the occurrence of some individuals within the sediments but cannot explain the isotopic variation between species occurring in the same interval. Microgradients in deep-sea sediment properties have been reported (e.g. Aller and Aller, 1986), and heterogeneity in microhabitats may affect the 6i3C value of benthic foraminfera tests (McCorkle et al., 1990; Loubere et al., 1995). The sediment depth ranges for many
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benthic foraminiferal taxa overlap (e.g. epifaunal, O-l cm; shallow infaunal, O-2 cm), and as a result, species that are categorized as having different microhabitat preferences may be found in a single sample (the same interval). The isotopic composition of each species generally agrees with its microhabitat preference, even when different species with different preferences are found in the same interval; epifaunal taxa have higher 613C values than shallow infaunal and transitional species (Fig. 12). In deeper sediment intervals, shallow infaunal and transitional taxa have higher values than deep infaunal taxa (e.g. Fig. 13). Since this isotopic ranking of species within the same sediment interval agrees in general with microhabitat preferences, we suggest that fine-scale heterogeneity of microenvironments within the intervals sampled accounts for this correlation and that the isotopic compositions of most taxa are related to the microhabitats where they secrete their tests. Intrageneric differences
Intrageneric isotopic differences are evident in Cibicidoides and possibly Uvigerina and Bulimina. Cibicidoides bradyi is a transitional taxa, living in sediment depths from O-4 cm, and C. wuellerstorfi (Planulina wuellerstorji) is an epifaunal species (Corliss, 1985, 1991), preferring a microhabitat elevated above the sediment-water interface (Lutze and Thiel, 1989). The 613C value of C. wuellerstorfi in core 10 is higher than those of C. bradyi, as would be expected based on their different microhabitat preferences (Table 3). The 613C of B. marginata (- 0.58%) and B. mexicana ( - 1.08%) from the same interval of core 12 indicate that there may be intrageneric differences among Bulimina species. If the 613C values with standard deviations > 0.05 of U. peregrina and U. proboscidea from the same surficial intervals in cores 12 and 3 are reliable (marked in parentheses in Table 3), there are intrageneric differences of at least 0.1-0.2X in Uvigerina. Oxygen isotopes
Average differences between 6i8O values of Sulu and South China Sea taxa and the 6’*0 at equilibrium with calcite in the surrounding bottom-waters are generally consistent with those reported in previous studies. The range of Aa’* in calcitic species from the Sulu and South China Seas is about 1.OL (Fig. 15). In the Sulu Sea, B. mexicana, 0. umbonatus, and U. proboscidea are closest to equilibrium with calcite (within 0.3X). Chilostomella oolina and U. Peregrina have average 6’*0 values within 0.3% of equilibrium calcite in the South China Sea. The relatively large standard deviation of C. pachyderma 6’*0 values results from the inclusion of the value from the 2.5-3 cm interval (the isotope value from this interval seems unusually high, but we saw no reason to exclude this measurement). Comparisons of the A6180 values of the two species which occur in more than one sample in both Sulu Sea and South China Sea isotopic data sets reveals that C. bradyi and U. proboscidea may have slightly higher Aal values (by about 0.2%) in the Sulu Sea. In each basin, however, these species have A.6180 values which are separated by about 0.1% (difference = 0.13 in the Sulu Sea, and 0.09 in the South China Sea). South China Sea species have As’*0 values which may be related to microhabitat preferences, but in contrast to the patterns noted by McCorkle et al. (1990), Sulu Sea data exhibit no trends in Ag’*O associated with microhabitat preferences. In the Sulu Sea, the aragonitic taxon, H. elegans, is enriched by about 0.4-0.6%0 in 6180 relative to Uvigerina species, and similar differences have been noted in previous studies (e.g. Grossman and Ku, 1986; McCorkle et al., 1990). In the South China Sea, the aragonitic taxon, C. paczjica is enriched by about 0.2-0.04%0
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relative to Uvigerina species, whereas G. lobatulusis depleted by about 1.2%0 relative to Uvigerina.This significant depletion in the al80 of G. lobaruh is unusual for an aragonitic taxon, but because of the lack of isotopic data for this species in other areas, comparisons are not possible. Acknowfedgements-We thank the crew and scientists aboard the R.V. Moanu Wavefor assistance during the Sulu Sea-South China Sea Cruise; E. Tappa, A. Bruce, K. Hicks, Aimee Dolan-Laughlin, M. Malone, M. Qingmin, and M. Fay for technical assistance; R. C. Thunell, T. C. Johnson, D. A. Livingstone, and P. A. Baker for examining an earlier version of the manuscript. Comments and suggestions included in the reviews by D. McCorkle and E. Grossman significantly enhanced the paper. We are grateful to M. Rutgers van der Loeff for providing pore-water oxygen data and to S. Kuehl and T. Fuglseth for providing sedimentation rate and mixing coefficient data. Helpful discussions with D. McCorkle, B. Opdyke, and M. Malone are also very much appreciated. Many thanks are due to Patrick De Deckker and the Australian Marine Quatemary Program in the Geology Department at the Australian National University for their support and hospitality during the senior author’s recent postdoctoral work in Canberra, Australia. This research was supported by National Science Foundation Grants OCE-8700744 and OCE-90-12581.
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