Bahasa
Halaman
Hukum
www.elsevier.com/locate/marmicro
Marine Micropaleontolog
A test of different factors influencing the isotopic signal of
planktonic foraminifera in surface sediments from the
northern South China Sea
Ludvig Lfwemarka,T, Wei-Li Honga,1, Tzen-Fu Yuib,2, Gwo-Wei Hungc,3
aDepartment of Geosciences, National Taiwan University, Taipei, Taiwan, ROCbInstitute of Earth Sciences, Academia Sinica, P.O. Box 55-1, 115 Taipei, Taiwan, ROC
cInstitute of Marine Geology and Chemistry, National Sun Yat-sen University, Kaohsiung, Taiwan 804, ROC
Received 12 October 2004; received in revised form 4 February 2005; accepted 4 February 2005
Abstract
The stable isotope composition of planktonic foraminifera is one of the most important proxies in paleoenvironmental
research. In this study, three parameters affecting the stable isotope values of Globigerinoides ruber from surface sediment from
the northern South China Sea were tested: different cleaning methods, different morphotypes, and different size fractions. Our
results show that in the small size fraction, there is a small but significant effect on y13C by oxidizing the tests prior to
measurement. Our data also confirm a small but significant difference between different morphotypes of G. ruber. However, the
variability caused by the seasonal effect stable isotope value is larger than the effect caused by different cleaning protocols or
different morphotypes. The large spread of the isotope values (up to 2x) have some implications to paleoceanographic
reconstructions; when measurements are performed on a small number of foraminiferal tests, the isotope value does not
necessarily reflect yearly average or a certain season but is a random value of the seasonal variability in that region.
D 2005 Elsevier B.V. All rights reserved.
Keywords: Planktonic foraminifera; Stable isotopes; South China Sea; Cleaning protocol; Surface sediment
0377-8398/$ - see front matter D 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.marmicro.2005.02.004
T Corresponding author. Previously at Institute of Earth Sciences,
Academia Sinica, P.O. Box 55-1, 115 Taipei, Taiwan, ROC.
Fax: +886 2 23636095.
E-mail addresses: [email protected] (L. Lfwemark),
[email protected] (W.-L. Hong), [email protected]
(T.-F. Yui), [email protected] (G.-W. Hung).1 Fax: +886 2 23636095.2 Fax: +886 2 2783 9871.3 Fax: +886 7 5255149.
1. Introduction
The stable isotope composition of planktonic
foraminifera is one of the most commonly used
paleoenvironmental proxies. The isotope ratio of
d18O is routinely used for the chronostratigraphic
framework of marine sediment records and also often
used for the reconstruction of parameters such as
marine water temperatures (e.g., Emiliani, 1955;
y 55 (2005) 49–62
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6250
Shackleton, 1967; Weaver et al., 1997), sea level/ice
volume changes (e.g., Hays et al., 1976; Shackleton,
1987; Bard et al., 1989), d18O of sea water and salinity
variations (e.g., Duplessy et al., 1992; Maslin et al.,
1995; Wang et al., 1995; Rohling, 2000; Lea et al.,
2003). Recent approaches include the use of differ-
ences in d18O between different species or regions to
infer changes in upper water structure and monsoon
intensity (e.g., Ganssen and Troelstra, 1987; Farrell et
al., 1995; Chaisson and Ravelo, 1997; Huang et al.,
2003; Wei et al., 2003; Rohling et al., 2004). Large
scale ocean circulation changes (e.g., Curry et al.,
1988; Duplessy et al., 1988; Sarnthein et al., 1994),
variations in the carbon cycle and the strength of the
biological pumping of carbon in the ocean (e.g.,
Ganssen and Sarnthein, 1983; Mortlock et al., 1991)
can be deduced from variations in d13C in planktonic
and benthic foraminifera. Because even small changes
in the isotope ratios may imply significant changes in
the environmental system, it is necessary to measure
the isotopic signals with the highest possible precision
and to exclude any sources of error.
Variations caused by different morphotypes of the
same species having different preferences for different
habitats (depths) and variations due the ontogenetic
development can be assessed by strict morphometric
criteria when selecting the tests and by the employment
of narrow size fractions. The fact that different species
show a slight offset in their fractionation compared to
what would be expected if they calcified in equilibrium
with sea water, the so called vital effect, has been
assessed through sediment trap and cultivation experi-
ments where the offset of the specific species is
measured (e.g., Erez and Honjo, 1981; Bouvier-
Soumagnac and Duplessy, 1985; Deuser, 1987).
Several studies have casually addressed the influ-
ence of different chemical treatments on the stable
oxygen and carbon isotope measurements of carbonate
materials (Duplessy, 1978, and references therein). For
example, Emiliani (1966) noted a lowering of up to
0.8x in the y18O of ground and Helium roasted calcite
from Tridacna shells, and a �0.2x change in y18O of
the planktonic foraminifera Globigerinoides sacculifer
due to oxidization with NaClO. A similar change was
observed by Savin and Douglas (1973) in Recent
planktonic foraminifera (y18O-0.29x, y13C-0.2x)
after exposure to NaClO. Particular attention has also
been given to the effect of different cleaning protocols
on the studies of aminoacids in foraminiferal organic
matter (Katz and Man, 1979) and Mg/Ca ratios in the
calcite shells (e.g., Martin and Lea, 2002). Further-
more, the storage of foraminiferal tests in formalin
solution resulted in a significant change in the stable
isotope values (Ganssen, 1981), and the comparison of
foraminifera ultrasonified in alcohol with untreated
ones displayed significantly heavier y18O and y13Cvalues, attributed to the removal of coccolith dust from
the tests (Voelker, 1999). However, to our knowledge,
no published study has systematically addressed the
impact of the most commonly used cleaning methods
on the stable isotope composition of foraminiferal
shells.
The purpose of this study is to test whether the
most commonly used cleaning methods have any
influence on the stable isotope values of planktonic
foraminifera, or if the cleaning is a pointless step,
actually increasing the risk of introducing errors. We
also compare the stable isotope values of different
morphotypes/sizes of Globigerinoides ruber, since
recent studies have given somewhat disparate results
(S. Steinke, pers. com., Lin et al., 2004) on the two
morphotypes distinguished by Wang (2000). A third
aim is to assess the isotopic variability of planktonic
foraminifera in surface sediments caused by seasonal
variations in surface water conditions and different
calcifying seasons.
2. Materials and method
2.1. Location and hydrography
The two box cores M1 (119827.98VE, 21825VN,2993 m water depth) and F (118835.03VE,20814.97VN, 2735 m water depth) used in this study
were taken from the north-easternmost South China
Sea during an Ocean Researcher I cruise in 2004 (Fig.
1). The sediment at these locations consists of
hemipelagic muds.
The surface water of the South China Sea is
characterized by the inflow of saline Western Philip-
pine Water through the Luzon strait that is mixed with
fresh river water from the surrounding land areas
(Wyrtki, 1961). The surface circulation in the basin is
controlled by the strong northeast monsoon driving a
cyclonic gyre over the whole basin during winter and
116° 118° 120° 122° 124°
20°
22°
24°
0 50 100
M1
F
18°
200m
1000m
2000m
3000m
4000m
km
Fig. 1. Bathymetric chart showing the locations of the box cores in the north-eastern South China Sea.
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–62 51
the weaker southwest monsoon driving an anticy-
clonic gyre, primarily in the southern part of the
basin, during summer (Wyrtki, 1961; Liang et al.,
2000). In the northernmost part of the South China
Sea the surface hydrography is especially complicated
due to the mixing of several distinctly different water
masses. In winter, warm saline Kuroshio-derived
water enters through the Bashi Strait, this water is
mixed with cold surface water entering from the
Taiwan Strait (Wyrtki, 1961). In summer, the hydrog-
raphy is dominated by warm waters from the southern
South China Sea (Shaw and Chao, 1994). Summer
conditions are usually oligotrophic and typhoons
mixing the upper surface can have a large impact
generating short term blooming events (Liu and Liu,
2002). In the northern South China Sea a sea surface
temperature difference of 5–6 degrees between winter
(~ 23 8C) and summer (~ 29 8C) is present (Levitus
and Boyer, 1994).
2.2. Sample preparation
The sample material was dispersed in distilled
water, and wet sieved with a 63 Am sieve until no
more fine material was released. The sieved material
was ultrasonified in tap water for a maximum of 30 s
in order to disperse clay aggregates and to loosen
adhering clay particles. The sample was wet sieved
again to remove the loosened material. The sediment
was flushed onto filter paper and dried at 45 8Covernight. The dried sample was dry sieved to
separate the size fractions 63–250 Am, 250–350 Am,
and N350 Am. Only the size fraction 250–350 Am was
used for this study. The planktonic foraminifera
Globigerinoides ruber was picked out under micro-
scope, and separated into three types according to
their morphology (Fig. 2). Morphotype I corresponds
closely to G. ruber sensu stricto (s.s.) of Wang (2000),
whereas morphotype II correspond to G. ruber sensu
lato (s.l.) of Wang (2000) and morphotype III
correspond to the kummerform of Hecht and Savin
(1972) and Hecht (1974). Morphotype II and III are
characterized by flattened and minute last chambers,
respectively. Each morphotype was subsequently split
into two size fractions, 250–297 Am, and 297–350
Am, to minimize the effect of ontogenetic changes in
stable isotope composition. Ten repetitive measure-
ments of stable oxygen and carbon isotopes on each
Fig. 2. Representative specimens of the three morphotypes of Globigerinoides ruber distinguished in this study. Morphotype I approximately
corresponds to the sensu stricto of Wang (2000), whereas morphotype II corresponds to G. ruber sensu lato (s.l.) of Wang (2000) and
morphotype III corresponds to the kummerform of Hecht and Savin (1972) and Hecht (1974). Morphotype II is characterized by a flattened and
asymmetrical last chambers and morphotype III is characterized by a minute last chamber.
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6252
size fraction of the three morphotypes were then
performed at the Institute of Earth Sciences, Aca-
demia Sinica using a Finnigan MAT252 mass
spectrometer with Kiel Device (Thermoquest-Finni-
gan). The machine precision of the mass spectrometer
measurements is F 0.03x for carbon isotopes and F
WetSieving
DrySieving
Set A
Set B
Set C
Set D
Set E
Foraminifers were separatedinto five groups
N
Fig. 3. The sediment was first washed over a sieve with a 63 Am mesh and
before 5–6 foraminiferal tests were measured on a Finnigan MAT252 m
different cleaning methods were applied to four subsets from each size fr
0.05x for oxygen isotopes measured on the in-house
standard (LB-32). All data are reported in x vs. the
PDB-standard. For each stable isotope measurement
five foraminiferal tests were used in the size fraction
297–350 Am and 6 tests in the smaller size fraction
250–297 Am.
MS
Oxidized with
aClO
Crack
Ultrasonic bath
inalcohol
then dry sieved into two size fractions (250–297 and 297–350 Am)
ass spectrometer. Additionally, on foraminifera from station F, four
action of the foraminifera before the isotope measurements.
Table 1
Station F
Morphotype I 297–350 Am 250–297 Am Station F 297–350 Am 250–297 Am
Untreated y13C y18O y13C y18O Morphotype II y13C y18O y13C y18O
A1 1.48 -2.84 1.10 -2.81 II1 1.72 -1.86 1.27 -2.27
A2 1.38 -3.16 1.38 -2.90 II2 1.75 -2.51 1.12 -2.41
A3 1.66 -2.64 1.39 -2.45 II3 1.71 -2.01 1.52 -2.35
A4 1.32 -2.48 1.70 -2.20 II4 1.59 -2.41 1.24 -2.36
A5 1.78 -2.37 1.36 -2.92 II5 1.60 -2.01 1.33 -2.34
A6 1.55 -2.53 1.14 -2.13 II6 1.49 -2.04 1.24 -2.11
A7 1.43 -2.69 1.40 -2.62 II7 1.57 -2.40 1.27 -2.73
A8 1.53 -3.38 1.21 -2.13 II8 1.67 -2.42 1.04 -2.58
A9 1.48 -2.59 1.42 -2.41 II9 1.52 -2.59 1.23 -2.52
A10 1.31 -2.94 1.12 -2.89 II10 1.65 -2.99 1.17 -2.42
AVG 1.49 -2.76 1.32 -2.54 AVG 1.63 -2.32 1.24 -2.41
STD 0.16 0.34 0.18 0.33 STD 0.06 0.33 0.13 0.17
Station F Station F
Cleaning method B y13C y18O y13C y18O Morphotype III y13C y18O y13C y18O
B1 1.42 -2.88 1.44 -2.68 III1 1.53 -2.27 0.91 -2.77
B2 1.23 -2.68 1.29 -2.46 III2 1.37 -2.92 1.22 -2.81
B3 1.19 -2.61 1.37 -2.91 III3 1.34 -2.69 1.08 -3.18
B4 1.22 -3.17 1.36 -2.41 III4 1.34 -2.53 1.43 -2.57
B5 1.59 -2.92 1.18 -2.85 III5 1.45 -2.84 1.29 -2.30
B6 1.62 -3.33 1.40 -2.08 III6 1.27 -2.46 1.50 -2.55
B7 1.65 -3.18 1.28 -2.72 III7 1.49 -3.14 1.36 -3.26
B8 1.24 -2.85 1.56 -2.70 III8 1.44 -2.62 1.41 -3.01
B9 1.19 -2.55 1.29 -2.86 III9 1.37 -2.77 1.61 -2.42
B10 1.51 -3.32 1.20 -2.69 III10 1.47 -3.04 1.64 -2.67
AVG 1.39 -2.95 1.34 -2.64 AVG 1.40 -2.69 1.35 -2.75
STD 0.21 0.29 0.11 0.25 STD 0.09 0.30 0.23 0.32
Station F Station M1
Cleaning method C y13C y18O y13C y18O Morphotype I y13C y18O y13C y18O
C1 0.95 -2.53 1.24 -2.33 M1-1 1.52 -3.16 1.35 -1.93
C2 1.37 -3.22 1.18 -3.07 M1-2 1.29 -3.10 1.54 -2.79
C3 1.32 -2.90 1.63 -3.13 M1-3 1.51 -3.18 1.21 -3.57
C4 1.47 -2.91 1.29 -2.82 M1-4 1.66 -3.07 1.33 -3.05
C5 1.23 -3.01 1.29 -2.57 M1-5 1.58 -3.29 1.48 -3.00
C6 1.59 -2.90 1.03 -2.59 M1-6 1.52 -3.84 1.39 -3.03
C7 2.31 -2.55 1.58 -2.92 M1-7 1.56 -3.07 1.42 -3.28
C8 0.62 -3.48 1.41 -3.28 M1-8 1.41 -2.94 1.60 -2.69
C9 1.16 -3.11 1.64 -2.85 M1-9 1.89 -3.01 1.47 -2.64
C10 1.40 -3.48 1.47 -2.63 M1-10 1.62 -2.78 1.34 -2.95
AVG 1.34 -3.01 1.38 -2.82 AVG 1.52 -3.24 1.39 -2.95
STD 0.51 0.33 0.20 0.29 STD 0.11 0.27 0.11 0.51
Station F
Cleaning method D y13C y18O y13C y18O
D1 * * 1.07 -2.40
D2 * * 1.05 -2.70
D3 1.08 -2.91 1.20 -2.22
D4 1.27 -2.90 1.30 -2.91
(continued on next page)
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–62 53
Table 1 (continued)
Station F
Cleaning method D y13C y18O y13C y18O
D5 1.50 -2.91 1.08 -2.60
D6 1.80 -2.28 1.33 -4.62
D7 1.38 -2.69 1.23 -2.67
D8 1.20 -3.24 1.13 -2.94
D9 1.50 -2.56 1.11 -2.71
D10 1.40 -2.67 0.94 -2.57
AVG 1.39 -2.77 1.14 -2.83
STD 0.22 0.35 0.12 0.66
Station F
Cleaning method E y13C y18O y13C y18O
E1 1.48 -2.64 1.02 -2.70
E2 1.48 -2.83 1.32 -2.79
E3 1.39 -2.48 1.07 -2.65
E4 1.34 -2.41 1.37 -2.97
E5 1.02 -2.73 1.05 -2.53
E6 1.52 -2.41 1.13 -2.96
E7 1.18 -2.85 1.26 -3.37
E8 1.20 -2.64 1.17 -2.51
E9 1.42 -3.31 1.19 -2.92
E10 1.43 -2.73 1.04 -2.74
AVG 1.35 -2.70 1.16 -2.81
STD 0.17 0.31 0.12 0.25
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6254
Additionally, on samples from station F, four
different cleaning methods were applied upon sub-
sets of the two size fractions of morphotype I. The
first cleaning method (set B) consists of cautious
ultrasonification in ethanol for 10 s and immediate
removal of the ethanol solution in order to remove
dispersed material. In the second method (C), the
tests were first cracked to expose their inner
chambers and then ultrasonified in ethanol. In the
third method (D), the tests were oxidized with
NaClO for 24 h in order to remove organic material
and then ultrasonified in ethanol. In the fourth
method (E), the tests were oxidized with NaClO,
cracked, and finally ultrasonified in ethanol (Fig. 3).
The cleaned foraminifera (10 repetitive measure-
ments of 5 or 6 foraminiferal tests for each set) were
then measured on the same mass spectrometer as the
untreated tests (Table 1).
2.3. Statistical evaluation
We used unpaired Student t-Test to test if there
is a significant difference between the untreated and
cleaned foraminifera, between the two size fractions,
between the two stations, and between the different
morphotypes. The unpaired Student t-Test is suit-
able in situations where the sample size is small,
the two groups of samples are independent, and
when the standard deviation of the population is
unknown. We used a two-tailed test with the
significant level 0.05.
3. Results
The distribution of the y18O values in morphotypes
I to III is quite large, with values ranging from �1.7xto �3.4x and �2.1x to �3.3x in the larger and
smaller size fractions, respectively (Fig. 4a). This
results in standard deviations around 0.3x. The
averages range from �2.4x to �2.8x. Morphotype
2 has highest y18O values in both size fractions. There
is a significant difference (a =0.05) between morpho-
type I and II, and between type II and III in size
fraction 297–350 Am, and between morphotype II and
III in the smaller size fraction. The y13C values of the
0.8
1.0
1.2
1.4
1.6
1.8
2.0
-3.5
-3.0
-2.5
-2.0
-1.5
III
IIII
II
III
297-350 µm 250-297 µm
250-297 µm297-350 µm
I
II
IIII
II
III
Different Morphotypes
δ18O
(per
mil)
δ13
C(p
erm
il)
a
b
Fig. 4. a) The y18O values of the different morphotypes of G. ruber in site F. The spread of the data points is larger than 1.5x. The averages of
morphotype II in both size fractions are heavier than for the other two morphotypes. In size fraction 297–350 Am, morphotype II is significantly
different from I and III. In size fraction 250–297 Am, morphotypes II is only significantly different from morphotype III. b) The y13C values of
the different morphotypes in site F. The spread is almost 1x, and in size fraction 297–350 Am, there is a significant difference between
morphotype II and the two other morphotypes.
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–62 55
different morphotypes also spread in a large range,
which is about 1.8x to slightly less than 1x (Fig.
4b). The averages range from 1.6x to 1.3x, with
standard deviations not larger than 0.22x. A signifi-
cant difference was found between morphotypes I and
II, and between II and III in the large size fraction. In
the smaller size fraction the differences between the
three morphotypes were smaller and not statistically
significant.
The y18O values of the different cleaning methods
also spread in a large range, from about �2.0x to
�3.5x, and the averages range from �2.5x to
�3x (Fig. 5a). Except for the group D in size
fraction 250–297 Am, where one extreme outlier is
observed at more than �4.5x, the standard devia-
tions are about 0.3x. In y18O, no significant differ-
ences between the untreated foraminifera (set A) and
the cleaned samples were detected. The range of y13Cvalues for the different cleaning methods is about 1x(1.8x–0.6x), and the averages range from 1.5x to
1.2x (Fig. 5b). The standard deviations generally are
about 0.2x, except for 297–350 Am, set C, where an
outlier causes an unusually large standard deviation.
We found significant differences between the
untreated and cleaning method E in both size
fractions and between untreated (A) and method D
in the smaller size fraction. This suggests an
influence of the oxidation step on the measured
y13C values.
Comparing the stable oxygen isotopes of the
foraminiferal tests from the two different sampling
sites F and M1, there is a significant difference in the
bigger size fraction. Although we do not find a
significant difference in the smaller size fraction, the
t-value was very close to the critical value. The y18Oaverages of the tests from these two sampling sites
are �2.8F0.4x (F) and �3.2F0.3x (M1),
respectively, in the size fraction 297–350 Am, and
�2.5F0.3x (F) and �2.9F0.5x (M1) in the
smaller size fraction (Fig. 6a). Thus, the northern
station M1 is about 0.4x lighter than station F. In
contrast, there is no significant difference between
0.5
1.0
1.5
2.0
2.5
AB
CD E A B C
D E
297-350 µm 250-297 µm
-5.0
-4.5
-4.0
-3.5
-3.0
-2.5
-2.0
-1.5
A B CD E
AB
C D E
297-350 µm 250-297 µm
Different Cleaning Methods
δ18O
(per
mil)
δ13C
(per
mil)
a
b
Fig. 5. a) The y18O values of the different cleaning methods. The spread is large and the averages of the different cleaning methods deviate from
the untreated sample by up to 0.3x. However, these differences are not statistically significant. b) The y13C values of the different cleaning
methods. The values spread almost 2x. In the smaller size fraction, methods D and E that include an oxidation step have significantly lower
y13C values than the untreated sample.
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6256
the two sampling sites in their y13C values. The
averages range from 1.5x to 1.3x with standard
deviations around 0.2x (Fig. 6b).
4. Discussion
Globigerinoides ruber is a subtropical, shallow
dwelling spinose planktonic foraminiferal species
commonly used in paleoceanographic reconstruc-
tions. This species lives in the photic zone of the
water column, primarily in the upper 50 m and
shows little daily vertical migration (Be, 1977). In
subtropical and transitional waters, G. ruber primar-
ily secretes its shell during the summer months,
therefore, the y18O of G. ruber in the sedimentary
record often is taken to reflect summer surface water
conditions (Deuser et al., 1981; Duplessy et al.,
1981; Ganssen, 1983). However, sediment trap data
from the South China Sea (Wiesner et al., 1996) and
the tropical western Pacific (Kawahata et al., 2002)
suggest that the maximum flux of G. ruber is not
necessarily bound to the summer season. Evidence
from sediment traps in the Saragasso Sea suggests
that the stable oxygen isotopes are subject to a vital
effect of about �0.20x relative to sea water
(Deuser, 1987). Due to the photosynthetic activity
of dinoflagellates living in symbiosis with foramin-
ifera, the calcareous tests of G. ruber are enriched in13C relative to sea water (Hemleben et al., 1989;
Bemis et al., 2000).
The repetitive measurements of stable isotopes on
Globigerinoides ruber in surface samples from the
northern South China Sea show three interesting
features. First, there is an unexpectedly large varia-
bility in the stable isotope measurements. Second,
there is a significant difference between different
morphotypes. Third, there is a statistically significant
difference in d13C between the tests exposed to an
oxidizing agent and the untreated tests, whereas the
other cleaning methods do not have any significant
effect.
δ18O
(per
mil)
δ13C
(per
mil)
1.0
1.2
1.4
1.6
1.8
2.0
-4.0
-3.5
-3.0
-2.5
-2.0
-1.5
F
M1
M1
M1
M1
F
F
F
297-350 µm
297-350 µm
250-297 µm
250-297 µm
Different Stationsa
b
Fig. 6. a) The difference in y18O values between the two sampling sites. The averages of site F are higher than site M1 in both size fractions.
There is a significant difference between these two sampling sites in the big size fraction, in the small size fraction the difference is large and
close to being significant. b) The difference in y13C values between the two sampling sites. The averages of site F are smaller than site M1, but
the differences are not statistically significant.
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–62 57
4.1. Stable isotope variability in the surface sediment
4.1.1. Variability in d18O values
The range of almost 1.5x observed in the
measured y18O values (Fig. 4) corresponds to a
temperature difference of 6–7 8C (e.g., Epstein et
al., 1953; O’Neil et al., 1969; Shackleton, 1974; Erez
and Luz, 1983). This agrees with the reported winter
and summer temperatures that range from around 23–
29 8C (Levitus and Boyer, 1994).
Because only 5 tests were used for the analysis, the
measured value does not necessarily represent a
yearly average. Rather, the value of each measurement
is the outcome of randomly mixed tests from different
seasons. Although it is unlikely to coincidentally pick
5 out of 5 tests with extreme winter or summer values,
there is a realistic chance of choosing 5 tests whose
average is much closer to typical winter or summer
values than yearly average. We therefore believe that
in our test of different cleaning methods, where 50
measurements were made in each grainsize fraction, it
is reasonable to assume that the lightest and heaviest
isotopes (the outliers) are close approximations of
typical (but not maximal) summer and winter temper-
atures, respectively. This interpretation is supported
by sediment trap data from the same region (Lin et al.,
2004). The heaviest winter values are slightly heavier
than �2x, compared to �1.8x in our surface
samples. Summer sediment trap values generally lie
around �3.5x, which is about the same as the lightest
points from our surface samples.
To avoid this kind of spread in the isotope values,
larger numbers of foraminiferal tests should be used.
The larger the number of tests used for each individual
measurement are, the smaller the chance of coinci-
dentally measuring only extreme tests should be and
the narrower the spread would be expected to be
(Schiffelbein and Hills, 1984).
The isotopic signal recorded in the surface sedi-
ment can also be further complicated by seasonal
variations in foraminiferal productivity. Sediment trap
data from the Saragasso Sea show a strong increase in
foraminiferal flux during the winter season (Deuser,
1987), which would bias any isotopic signal toward
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6258
isotopic conditions reflecting that season. In contrast,
sediment trap experiments from the western equatorial
Pacific do not display such a strong seasonality
(Kawahata et al., 2002). However, that study also
showed that the connection between phytoplankton
productivity and foraminiferal test flux is not as strong
as might be expected. Therefore, absolute fluxes of
the specific species are needed to accurately assess the
influence of variations in foraminiferal flux on the
average isotope signals. In the South China Sea the
foraminiferal productivity shows a more variable
pattern with several peaks during summer as well as
winter monsoon regimes (Wiesner et al., 1996). Thus,
the average, if sufficient foraminiferal tests are used,
could be expected to represent yearly average.
There is a significant difference in the average
y18O values between the two stations, the northern
station M1 being approximately 0.4x lighter than
station F, indicating up to two degrees warmer surface
waters. Whereas summer sea surface temperatures are
largely uniform in the South China Sea, the winter
temperatures generally decreases with increasing
latitude (Levitus and Boyer, 1994). We attribute the
observed discrepancy to the winter time intrusions of
warm Kuroshio water (Wyrtki, 1961) that would have
a stronger influence on the northern station resulting
in lighter y18O-values.
4.1.2. Variability in d13C Values
Although the size of the spread observed in y13Cfrom surface sedimentGlobigerinoides ruber is similar
to the one observed in sediment traps from the same
region (Lin et al., 2004), there is an offset of about 1xbetween the two data sets. Whereas most surface
sediment values fall between 1 and 2x, the sediment
trap data fall between 0 and 1x. The sediment trap data
show a clear seasonal variability with high y13C values
during the summer months and low values in the
winter. Lin et al. (2004) interpreted this as an effect of
seasonal variations in surface water productivity. A
number of studies have shown a positive correlation
between primary productivity and y13C of the phyto-
plankton (e.g., Deuser, 1970; Sarnthein et al., 1988).
The enhanced removal of organic carbon relatively rich
in 13C during the winter season results in lighter y13Cseawater values and subsequently lighter foraminiferal
calcite, and vice versa for the summer months. Ship-
board and CZCS-SeaWiFS data confirm high nutrient
levels in the northern South China Sea in winter and
low during summer (Liu et al., 2002), corroborating the
view that it is the increased primary productivity in the
winter season that leads to an isotopically lighter y13C-signal in the planktonic foraminifera. The 1.5x range
in y13C observed in the G. ruber from the surface
sample therefore is interpreted as the seasonal range of
y13C in the seawater, the heaviest values representing
summer and the lightest representingwinter conditions.
The offset of about 1x between our surface sample
and the sediment trap data presented by Lin et al.
(2004) most likely is due to the Suess effect (Suess,
1965). The combustion of fossil fuels has raised the
atmospheric CO2 level from its preindustrial level
around 280 ppm and a y13C value of�6.5x (Friedli et
al., 1986) to the present 375 ppm with a y13C value
around �8x (Whorf and Keeling, 1998; Keeling and
Whorf, 2004). This introduction of anthropogenic,
isotopically light carbon has been shown to result in an
offset of almost�1x between plankton from the water
column and core top foraminifera in the Arctic Ocean
(Bauch et al., 2000). Variations in seawater carbonate
ion concentration (carbonate ion effect) have also been
shown to cause changes in the y13C of planktonic
foraminifera (Spero et al., 1997; Russell and Spero,
2000). Because the uppermost centimeters of the
sediment have been homogenized by bioturbation,
the foraminiferal tests sampled from the surface sedi-
ment represent a mixture consisting of primarily
preindustrial foraminifera and a mixture of foramin-
ifera from different seasons.
4.1.3. Influence of seasonal variations on downcore
reconstructions
The large variability observed in the y18O and y13Cvalues from the surface samples have some implica-
tions to the interpretation of downcore foraminiferal
data in paleoceanographic reconstructions when small
sample sizes are used. When large sample sizes are
used for the stable isotope analysis, the isotope value
measured will be close to the true average of the
mixed, multi-annual foraminiferal assemblage at that
level. Depending on whether planktonic foraminiferal
production is even over the year or concentrated to a
certain season the measured value will correspond to
yearly average or season specific conditions, respec-
tively. When sample sizes decrease, however, the
measured value no longer represents the average but a
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–62 59
random value following a normal distribution between
two extreme values. Our surface sample data clearly
reflect this phenomenon with most of the values
relatively close to the average but with a noteworthy
portion of the measurements close to the extreme
values predicted from sediment trap data. Thus, a
large part of the variability observed in downcore
records is not due to climatic variability or preparation
related errors, but simply reflects the regional seasonal
variability.
4.2. Size fractions and ontogenetic effects on d13C and
d18O
Although the size fraction analyzed was chosen to
only include adult stages of Globigerinoides ruber, a
significant difference in y13C between the small and
large size fractions in morphotypes I and II was
observed. The smaller size fractions are about 0.2xand 0.4x lighter than the larger foraminifera in
morphotypes I and II, respectively. The photosynthetic
activity of the dinoflagellates living in symbiosis with
the foraminifera have been shown to cause an enrich-
ment of 13C in the calcite shell relative to sea water
y13C (Hemleben et al., 1989; Bemis et al., 2000).
This could be interpreted as a difference in vital
effect or habitat between morphotypes I/II, and
morphotype III. However, no significant difference
was observed between the smaller and the larger tests
in d18O values. We therefore speculate that the vital
effects of morphotypes I and II are slightly different
from morphotype III. In morphotypes I and II the
symbiotic activity of the dinoflagellates play a more
important role in the larger specimen, i.e. later in the
life cycle, resulting in an enrichment in y13C relative
to the smaller ones. In morphotype III no such trend
was observed.
4.3. Different morphotypes
The differences in y18O and y13C between mor-
photype I and II, and II and III in the larger size
fraction seem to corroborate the view of Wang (2000)
that there are some differences between the particular
morphotypes. The heavier y18O values of morphotype
II, corresponding to bsensu latoQ of Wang (2000), also
agree with the notion that Globigerinoides ruber s.l.
lives at a deeper level than does G. ruber s.s.
Although the heavy values in the smaller size fraction
are not statistically significant, they still indicate a
deeper habitat. Therefore, morphotype II probably
calcifies in sub-surface waters of 30–50 m depth as
suggested by Wang (2000). CTD studies from the
northern South China Sea show a 2–3 8C decrease and
a 0.20–0.25 psu salinity increase, resulting in about
0.4x heavier y18O values (Wang, 2000), in agreement
with the ca 0.5x difference observed in our data. The
larger size fraction of morphotype II also differs from
morphotypes I and III in y13C, possibly indicating a
different habitat. We cannot exclude, however, that the
differences observed are due to differences in vital
effect or in preferential calcification season. The lack
of a statistically significant difference in the stable
isotopes of the small size fraction might indicate that
the observed differences in the larger foraminifera are
related to the ontogeny of the foraminifera and that
differences are smaller in earlier stages of the life
cycle. Wang (2000) used the somewhat larger size
fraction 315–400 Am for his study, thus no compara-
tive information about the smaller size fraction is
available.
4.4. The effect of different cleaning methods on stable
isotope values
The first two cleaning methods, cleaning in
ultrasonic bath, and cracking combined with cleaning
in ultrasonic bath were not statistically significant
different from the untreated foraminifera. This
suggests that if the sieving procedure was performed
adequately and the foraminiferal tests look clean
under optical microscope, i.e., no material visible in
the apertures, then a second cleaning through
cracking and/or ultrasonification in alcohol is not
necessary. Presumably, if no contaminating material
is visible in the apertures or adhering to the
foraminiferal shell, then the potential level of
contamination is small and the risk of losing material
or introducing an error during the different cleaning
steps probably outweighs the presumed benefits of
the cleaning. Especially the cracking step, where
primarily the outer chambers are cracked open, may
result in the loss of carbonate material that is sucked
out together with any dispersed coccolith material.
Because the early chambers secreted during juvenile
and neanic stages were produced under different
L. Lowemark et al. / Marine Micropaleontology 55 (2005) 49–6260
conditions (diet and probably also vital effect
changed during the ontogeny of the foraminifera
(Hemleben et al., 1989)), the loss of calcite from the
outer chambers may lead to an unwanted shift in
stable isotope values toward values representative of
earlier stages of the ontogeny.
In contrast, the two cleaning methods involving
oxidation of the foraminiferal tests with sodium
hypochlorite show an offset in y13C of about �0.4xto the untreated foraminifera. This offset is statistically
significant (95% confidence) in the smaller size
fraction and in set E (oxidation, cracking, and ultra-
sonification) of the larger size fraction, but not
significant in set D (297–350 Am, oxidation and
ultrasonification). No significant difference in y18Owas observed between the untreated and the oxidized
foraminifera. The negative offset is a surprise. Because
the oxidation step is introduced in order to remove any
remaining organic material and marine organic matter
generally has y13Corg values around �20x, the
removal of any remaining organic matter would be
expected to cause a positive shift in the y13C.In order to better determine the effect of the
different cleaning methods additional experiments
performed on planktonic foraminifera from a region
with minimal seasonal difference in surface water
conditions are needed. This would reduce the varia-
bility caused by the mixing of foraminifera that
calcified under different seasons.
5. Conclusions
The large spread of both y18O and y13C in the
measured surface samples show that when small
samples are used, the obtained values do not
necessarily represent yearly average or a certain
season. Rather, the values will randomly fall some-
where between seasonal maxima and minima. The
measured values will approximately follow a normal
distribution with most values close to the average but
with a not neglectable portion of the measurement
falling close to the extremes. The smaller the number
of foraminiferal tests used, the larger the chance of
values significantly deviating from the average.
The measured differences between different mor-
photypes corroborate the view of Wang (2000) that
Globigerinoides ruber sensu lato (our morphotype II)
calcifies at a larger depth during its adult stage than
does G. ruber sensu stricto (our morphotype I).
Finally, our experiment with applying different
cleaning methods prior to stable isotope analysis
shows that for clean samples, the commonly applied
ultrasonification in alcohol (sometimes combined with
a cracking of the outer chambers) does not have any
effect on neither y18O nor y13C values. In contrast, the
steps involving oxidation of the calcite shells with
sodium hypochlorite resulted in a statistically signifi-
cant lowering of the y13C values. Unless the
foraminiferal tests are visibly contaminated by cocco-
liths or adhering clay, cracking and/or ultrasonifica-
tion are unnecessary steps. However, a more detailed
study ought to be performed on surface samples from
a region characterized by minimal seasonal variations
in order to allow a better quantification of the
potential effects of different cleaning methods.
Acknowledgements
Special thanks to Yoshiyuki Iizuka (IESAS) for the
SEM pictures and Rosa Cheng (IESAS) for operating
the mass spectrometer. We thank Stephan Steinke
(Bremen University) for valuable discussions and for
his constructive help with an earlier version of this
paper. Mark Maslin (University College London) and
Gerald Ganssen (Vrije Universiteit Amsterdam) are
cordially thanked for their constructive reviews of a
previous version of this paper. We thankfully appre-
ciate economic support by the APEC-program and
Academia Sinica, Taiwan.
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