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APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Nov. 2011, p. 7479–7489 Vol. 77, No. 210099-2240/11/$12.00 doi:10.1128/AEM.00580-11Copyright © 2011, American Society for Microbiology. All Rights Reserved.

Spatial Variations in Archaeal Lipids of Surface Water and Core-TopSediments in the South China Sea and Their Implications for

Paleoclimate Studies�†Yuli Wei,1 Jinxiang Wang,1,2 Jie Liu,1 Liang Dong,1 Li Li,1* Hui Wang,1 Peng Wang,1

Meixun Zhao,3 and Chuanlun L. Zhang1,4*State Key Laboratory of Marine Geology, Tongji University, Shanghai 200092, China1; School of Earth Resources,

China University of Geosciences-Wuhan, Wuhan 430074, China2; Institute of Marine Organic Geochemistry,Ocean University of China, Qingdao 266100, China3; and Department of Marine Sciences,

University of Georgia, Athens, Georgia 306024

Received 14 March 2011/Accepted 16 August 2011

The South China Sea (SCS) is the largest marginal sea of the western Pacific Ocean, yet little is known aboutarchaeal distributions and TEX86-based temperatures in this unique oceanic setting. Here we report findingsof abundances in both core lipids (CL) and intact polar lipids (IPL) of Archaea from surface water (CL only)and core-top sediments from different regions of the SCS. TEX86-derived temperatures were also calculated forthese samples. The surface water had extremely low abundances of CL (average of 0.05 � 0.13 ng/liter; n � 75),with higher values present in regions where upwelling is known to occur. The core-top sediments had CL valuesof 0.1 to 0.9 �g/g, which are on the low end of CL concentrations reported for other marine sediments and mayreflect the oligotrophic nature of the open SCS. The IPL of Archaea accounted for 6 to 36.4% of total lipids (CLplus IPL), indicating that the majority of archaeal lipids in core-top sediments were derived from nonlivingcells. The TEX86-based temperatures of surface water were overall lower than satellite-based sea surfacetemperatures or CTD-measured in situ temperatures. The core-top sediment samples, however, had TEX86temperatures very close to the mean annual sea surface temperatures, except for samples with water depths ofless than 100 m. Our results demonstrated low and heterogeneous distributions of archaeal lipids in surfacewater and core-top sediments of the SCS, which may reflect local or regional differences in productivity ofArchaea. While TEX86-based temperatures for core-top marine sediments at deep water depths (>100 m)generally reflected mean annual sea surface temperatures, TEX86 temperatures in surface water varied basinwide and underestimated sea surface temperatures in most locations for the season when surface watersamples were collected.

The ocean contains a daunting number of Archaea, whichamount to approximately 1028 cells (30). This huge biomass,however, was unaccounted for 20 years ago and has attractedincreasing attention to the roles of these organisms in carbonand nitrogen cycles in the global ocean (see, e.g., references 13,25, and 49). One unique aspect of Archaea is their membranelipids, which are sensitive to temperature variations and havebeen used to develop paleotemperature proxies (31, 32, 55).Planktonic Archaea are also known to participate in ammoniaoxidation, thus playing an important role in the nitrogen cyclein the ocean (49).

The South China Sea (SCS) is the largest marginal sea of thewestern Pacific Ocean and belongs to the “East Indies Trian-gle,” which is the center of the maximum species diversitywithin the world’s largest biogeographic region, the tropicalIndo-West Pacific (6). The basin of the SCS is characterized byoligotrophic conditions, a shallow mixed layer and nutricline,low primary production (41), and low export production (8).

The climatic system of the SCS is affected by the proximityto the Tibetan Plateau and Pacific warm pool and character-ized by the East Asian monsoons. As a result, the SCS is oneof the best places for paleoclimate studies. Furthermore, theSCS has the most suitable conditions for high-resolution pale-oceanographic studies because of high sedimentation rates andgood carbonate preservation (64). The SCS is also highly suit-able for examining the relationships between continentalweathering, productivity, and climate, as three of the largestrivers in the world (from north to south, the Pearl River, theRed River, and the Mekong River) provide detrital fluxes tothe basin of the SCS (61).

Numerous paleoclimate studies have been conducted in theSCS, which are commonly based on temperature proxies suchas oxygen isotope ratios and Mg/Ca ratios of foraminifera,foraminiferal transfer function, or the U37

K methods (27, 28,67). It has been realized that individual temperature proxies allcan suffer from some biases (2), and the ideal approach wouldbe the integration of multiple proxies for addressing the samequestion (12). The TEX86 proxies have been developed onlyrecently (31, 32, 55) and most successfully used for marinesystems (see, e.g., references 5, 7, 11, and 43). In terrestrialenvironments, the TEX86 proxies have been successfully ap-plied to paleoclimate studies of some large lakes (4, 51, 52).

Despite the importance of the SCS in studies of primary

* Corresponding author. Mailing address: State Key Laboratory ofMarine Geology, Tongji University, Shanghai 200092, China. Phone:86-21-65982215. Fax: 86-21-65988808. E-mail for Li Li: [email protected]. E-mail for Chuanlun Zhang: [email protected].

† Supplemental material for this article may be found at http://aem.asm.org/.

� Published ahead of print on 2 September 2011.

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production and paleoclimate, little research has been doneregarding the abundance and community structure of Archaeaand the application of archaeal lipids as temperature proxies inthe SCS. In this study, we performed archaeal and bacterialglycerol dibiphytanyl glycerol tetraether (GDGT) analyses ofboth the core lipids (CL) and intact polar lipids (IPL) fromboth surface water and core-top sediments of the SCS. Ourdata for the core-top sediments from water depths of greaterthan 100 m showed that TEX86-derived sea surface tempera-tures (SST) based on CL matched annual mean sea surfacetemperatures from the satellite data, whereas TEX86-derivedsea surface temperatures based on surface water samples col-lected in April and May 2010 were lower than satellite-basedor CTD-determined sea surface temperatures for thosemonths. This study is the first calibration between satellite seasurface temperatures and TEX86-derived temperatures in theSCS, which may provide a reference for studies of paleoclimatechanges in the SCS using these proxies.

MATERIALS AND METHODS

Sample collections. (i) Water column sampling. A cruise in the SCS was madeon 23 April to 26 May 2010 by using the R/V Shiyan No. 3 of the South China SeaInstitute of Oceanology, Chinese Academy of Sciences. A total of 89 samplingstations were visited (Fig. 1), among which 78 stations were sampled for archaeallipids from the surface water (5- to 10-m water depths). At each location,filtration of seawater was conducted using a submersible pump, which was con-nected to a filtration system that contained three parallel and identical glass fiberfilters (142-mm diameter) with the same pore size (0.7 �m). The total volume ofwater for all three filters was recorded, and the filters were collected using sterilestainless steel forceps into 50-ml sterile Falcon tubes. The tubes were immedi-ately stored in a �20°C freezer on board the R/V Shiyan No. 3 after collection,transported under ambient temperature within 3 h, and stored at �80°C untilfurther analysis.

(ii) Core-top sediment sampling. Sediment samples were collected using cor-ing devices during three cruises in the SCS (Fig. 1). Cores A9, A7, and A5 wereretrieved in July 2009 using the R/V Dongfanghong No. 2, core HQ08-48PC wascollected in 2008 using the R/V Haiyang No. 4, and cores MD05-2894 to MD05-2905 were obtained during the Chinese-French joint Marco Polo/Images 147cruise in 2005 using the R/V Marion-Dufresne. The lengths of these cores wereless than 10 m. On board, the cores were opened and subsamples for lipid andmicrobiological studies were taken from the centers of the cores under sterile

FIG. 1. Map showing stations at which surface water was collected (open squares) and locations where sediment cores were collected (solidcircles) in the South China Sea. (Adapted from reference 64a with kind permission from Springer Science�Business Media.)

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conditions and stored in airtight sterile PVC tubes in a �20°C freezer. Sub-samples for chemical measurements were taken from the core, packed withaluminum foil, and then stored in cloth bags in a �20°C freezer. Only thecore-top sediments (�5-cm depths) were used for this study.

Concentration and isotopic compositions of TOC. About 5 g of sediment wasdecarbonated using 10% HCl and neutralized by repeated washing with distilledand deionized water before analysis. Part of the dried bulk sediment was used foranalysis of total organic carbon (TOC). The concentrations of TOC were deter-mined with an EA1110 organic element analyzer (Carlo Erba). The carbonisotopes of the TOC were then determined on a GV-Isoprime EA IRMS with aprecision of 0.1‰ for �13C (referenced to the Vienna Pee Dee Belemnite[VPDB]), which is defined as �13C � [(13C/12C)sample/(13C/12C)standard � 1] �1,000.

Lipid analyses. (i) Lipid extraction and fractionation. Three methods wereused for extraction of total lipids. In all three methods, the original sample wasspiked with an internal standard (C46, 974.08 ng) before the extraction procedurebegan. Method A was used for core HQ08-48PC. In this method, the freeze-dried sediment sample spiked with the internal standard was extracted ultrason-ically five times with a mixture of dichloromethane (DCM) and methanol(MeOH) (3:1, vol/vol). The total extract was transferred into a KOH-MeOHsolution (6%), left overnight, and then extracted with n-hexane five times.Method B was used for cores A9, A7, and A5. The freeze-dried sediment samplewas ultrasonically extracted three times with MeOH, three times with DCM-MeOH (1:1, vol/vol), and three times with DCM, and all extracts were combined.Method C was used for all filter samples, which produced core lipid only. In thismethod, the freeze-dried filter material was cut into small pieces using sterilizedscissors and then put into a 40-ml tube. MeOH, MeOH-DCM (1:1, vol/vol), andDCM were then used to extract lipids from the filter material sequentially, witheach step repeated at least once. Extract from each step was collected, and thetotal extract was transferred into a KOH-MeOH solution (6%), left overnight,and extracted with n-hexane five times (22).

The final extract obtained from each method was fractionated into apolar andpolar fractions using the same procedure. Briefly, the total extract was pouredinto a glass pipette column filled with activated silica gel and sequentially elutedwith hexane-DCM (9:1, vol: vol) to obtain the apolar fraction and with DCM-MeOH (1:1, vol/vol) to obtain the polar fraction. To obtain the core GDGTs(C-GDGTs), the polar fraction was filtered through a 0.45-�m polytetrafluoro-ethylene (PTFE) filter and directly injected onto a liquid chromatograph-massspectrometer (LC-MS). The intact polar GDGTs (IP-GDGTs) were indirectlyobtained as described by Huguet et al. (22). Briefly, half of the polar fraction wasdried under N2 and hydrolyzed with 5% (vol/vol) HCl in MeOH for 4 h at 70°C.The hydrolyzed GDGT fractions were sequentially extracted four times withDCM–Milli-Q water (1:1) and four times with Milli-Q water after hydrolysis wascomplete. Each extraction was followed by centrifugation, and all extracts werepooled into one sample. The extracts were dried under N2 and dissolved in 300�l n-hexane–isopropanol (99:1, vol/vol) before analysis by LC-MS. The IPL werecalculated as the difference between the yields after and before hydrolysis (22).

(ii) GDGT analysis and quantification. Analyses of GDGTs were performedat Tongji University by a slightly modified method of Schouten et al. (56).Separation was performed using an Agilent 1200 liquid chromatograph equippedwith an automatic injector and a Prevail Cyano column (2.1 by 150 mm, 3 �m;Alltech, Deerfield, IL), maintained at 40°C. The GDGTs were first eluted iso-cratically with n-hexane and isopropanol as follows: 99% n-hexane and 1%isopropanol for 5 min and then a linear gradient to 1.8% isopropanol in 45 min.The flow rate was 0.2 ml/min. After each analysis, the column was cleaned byback flushing n-hexane–isopropanol (90:10, vol/vol) at 0.2 ml/min for 10 min.Detection was performed using an Agilent 6460 triple-quadrupole mass spec-trometer (MS) with an atmospheric pressure chemical ionization (APCI) ionsource. Conditions for APCI MS were as follows: nebulizer pressure, 60 lb/in2;vaporizer temperature, 400°C; drying gas (N2) flow, 5 liters/min; temperature,200°C; capillary voltage, �3.5 kV; corona, 5 �A (3.2 kV). The single-ion mon-itoring (SIM) mode was used to detect eight isoprenoidal and branched GDGTsignals (m/z 1302, 1300, 1298, 1296, 1292, 1050, 1036, and 1022), one diethersignal (m/z 653), and the C46 internal standard (m/z 744), with a dwell time of 237ms per ion. The analytical error for TEX86 determined by replicate analysis wasbetter than �0.008 for all samples, which corresponded to about �0.4°C accord-ing to Kim et al. (31).

(iii) Calculations of GDGT proxies. TEX86 and TEX86H were calculated as

follows (32, 55): TEX86 � (GDGT-2 � GDGT-3 � GDGT-5)/(GDGT-1 �GDGT-2 � GDGT-3 � GDGT-5) and TEX86

H � log[(GDGT-2 � GDGT-3 �GDGT-5)/(GDGT-1 � GDGT-2 � GDGT-3 � GDGT-5)]. TEX86-derived seasurface temperatures (SST) were calculated according to three different equa-tions. Equation 1 is from Schouten et al. (55), who originally used a limited

number of core-top samples. Equation 2 is from Kim et al. (31), who updated theproxy of Schouten et al. (55) using an extended number of samples globally.

T � 66.7 � TEX86 � 18.67 (1)

T � 56.2 � TEX86 � 10.78 (2)

The third equation is according to Liu et al. (43): T � 50.47 � 16.33/TEX86.Kim et al. (32) also developed an equation (equation 3) which is suitable for

the reconstruction of SST in nonpolar oceans:

SST � 68.4 � TEX86H � 38.6 (3)

where TEX86H is the logarithmic function of TEX86. This equation was also used

to calculate sea surface temperatures from core-top samples in the SCS.A ring index (RI) was calculated for both CL and IPL as described by Pearson

et al. (50): RI � [(% GDGT-1) � 2 � (% GDGT-2) � 3 � (% GDGT-3) � 4 �(% GDGT-4) � 5 � (% GDGT-cren) � (% GDGT-cren-isomer)]/100.

Another proxy used in this study is the BIT (branches isoprenoidal tetra-ethers), which defines the input of terrestrial organic matter to the ocean (17):BIT � (I � II � III)/(I � II � III � GDGT-5).

(iv) Statistical analysis. Cluster analyses were performed using the relativeabundances of archaeal GDGTs to evaluate the relationships among lipid com-positions. The dendrogram of the cluster analysis was constructed with the Rprogramming language software (freeware available at http://cran.r-project.org/[44]) using Euclidean distance measure and ward linkage.

(v) Satellite data. The satellite-derived SST were obtained from the best SST(bSST) data sets from the NOAA advanced very-high-resolution radiometer(AVHRR) (version 5.0; http://pathfinder.nodc.noaa.gov) on a 4-km spatial res-olution. For the core-top sediment samples, we extracted and averaged theannual mean bSST for the 5 years between 2004 and 2009 using MATLAB. Forthe surface water samples collected during April and May 2010, we used themean surface temperature for the same months of 2009.

RESULTS

Basic physical/chemical conditions for surface water andsurface marine sediments. The water depth ranged from 42 mto 4176 m for stations at which surface filter samples werecollected (see Table S1 in the supplemental material). Waterdepths for core-top sediment samples ranged from 33 m to3,697 m (Table 1). Water chemistry was not available for thefilter samples, and pore water chemistry of the core-top sedi-ments was determined only for the HQ core. The concentra-tion of total organic carbon (TOC) ranged from 0.18% to1.36%, with an average value of 0.94% � 0.33% (n � 11). The�13C of TOC ranged from �19.54‰ to �24.2‰, with anaverage value of �21.21‰ � 0.33‰ (n � 11), which is in-dicative of marine primary production (26, 46).

Abundances and distributions of archaeal lipids (CL andIPL). (i) Surface water samples. At each station, 200 to 1,100liters of water was filtered. The abundances of total archaealCL were all above the detection limit of the instrument (0.8pg). However, 21 out of the 78 total filter samples gave verylow yields based on the examination of the internal stan-dard; these samples were eliminated from further analysis.The remaining samples showed total archaeal CL concen-trations ranging from 0.001 ng/liter to 0.894 ng/liter of sea-water (see Table S1 in the supplemental material). Highvalues (concentrations above 0.1 ng/liter) were observednear Hainan Island and the east coast of Vietnam and in thecentral basin or the Bashi Strait between Taiwan and thePhilippines; on the other hand, low archaeal CL concentra-tions commonly occurred in the southeast side of the SCS(Fig. 2). Overall, there is no correlation between concentra-tions of total archaeal CL and water column depths, asdemonstrated by the presence of high values in waters of all

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depths (Fig. 3). The concentrations of branched tetraetherlipids indicative of bacteria were generally below the detec-tion limit in the filter samples and thus were not reported.

(ii) Sediment samples. In sediment samples, total archaealCL ranged from 0.11 �g/g to 0.90 �g/g, with the highest valueoccurring in the shallow water depth (A7, 73 m) (Fig. 4). Totalarchaeal IPL ranged from 0.02 �g/g to 0.16 �g/g, with thehighest value occurring at MD05-2896 of the deep water (Ta-ble 1). Similar to the case for the filter samples, high total

archaeal CL occurred in both shallow (�200-m) and deep(1,000-m) waters, and the highest abundance also occurredin the shallower sediments (Fig. 4).

Total branched CL ranged from 3.14 ng/g to 38.72 ng/g, withthe highest value occurring at the shallowest water depth (A9,33 m) (Table 1). Total branched IPL ranged from 0.88 ng/g to13.24 ng/g; the highest value occurred at the same location(MD05-2896) where the highest archaeal IPL occurred.

Relative abundances of GDGTs in CL and IPL. (i) Filtersamples. GDGTs of archaeal CL were dominated by crenar-chaeol (25.1% to 65.0%) and GDGT-0 (4.2 to 45.5%) (seeTable S1 in the supplemental material). No archaeol (diether)(see Appendix for an explanation of structures) was detectedin filter samples. Cluster analysis of the relative GDGT distri-butions showed no grouping of filter samples according todepth (Fig. 3), suggesting that water depth is unlikely to be afactor affecting the distribution of archaeal lipids in the surfacewater of the SCS.

(ii) Sediment samples. The highest abundances of archaealGDGTs in either CL or IPL were also crenarchaeol (35.12 to69.73%) and GDGT-0 (16.20 to 31.69%). For the same sam-ple, crenarchaeol was consistently lower in relative abundancein IPL than in CL, whereas GDGT-0 was consistently higher inIPL than in CL. Archaeol was also higher in IPL than in CL inall but one sample (A7). Other GDGT compounds were eitherhigher or lower in IPL than in CL; however, the majority ofGDGT-2 and GDGT-3, and to a less extent, GDGT-1 andGDGT-4, showed higher values in IPL than in CL (Table 2).The ring index had a range of 2.28 to 3.70, with the IPL ringindex being 0.20 to 1.37 units higher than the CL ring index(Table 2). However, there was no correlation between CL- andIPL-derived ring indices (data not shown), suggesting differentGDGT compositions in the two lipid pools.

Cluster analysis showed that the compositions of the ar-chaeal CL GDGTs at shallower (�100-m) water depths weredifferent from those at water depths of below 1,000 m. Withinthe deep-water cluster, however, no spatial patterning was ob-served across the basin (Fig. 4). Comparison of the A9, A7, and

TABLE 1. General physical/chemical properties, total core lipids, and intact polar lipids, of archaea and bacteria of surface sediment samplesfrom the South China Sea

Parameter

Value at station:

MD05-2894

MD05-2896

MD05-2898

MD05-2900

MD05-2902

MD05-2903

MD05-2905 HQ08-48PC A5 A7 A9

Latitude (N) 07°02.25 08°49.50 13°47.39 14°23.33 17°57.70 19°27.32 20°08.17 16°57.5134 20°59.746 21°30.199 22°00.50Longitude (E) 111°33.11 111°26.47 112°11.03 110°41.74 114°57.33 116°15.15 117°21.61 110°31.5809 114°58.784 114°30.040 113°59.963Water depth (m) 1,982 1,657 2,395 1,455 3,697 2,066 1,647 1,474 102 73 33Sand content (%) 0.3 0.0 0.6 0.0 5.8 0.4 0.7 0.0 10.7 3.3 1.5Silt content (%) 70.2 70.7 74.3 77.3 75.5 76.7 82.4 82.1 79.3 82.0 80.1Clay content (%) 29.5 29.3 25.1 22.7 18.7 22.9 16.8 17.8 10.1 14.7 18.3Total organic

carbon (%)1.11 1.32 0.97 1.09 1.36 1.01 1.07 0.70 0.18 0.79 0.77

�13Corg (‰) �20.78 �19.95 �19.59 �20.66 �20.53 �20.98 �21.05 �21.47 �24.20 �22.30 �21.80Total archaeal

CL (ng/g)0.41 0.28 0.27 0.32 0.13 0.11 0.25 0.59 0.29 0.90 0.77

Total archaealIPL (ng/g)

0.05 0.02 0.16 0.05 0.04 0.02 0.04 NDa 0.06 0.06 ND

Total branchedCL (ng/g)

10.07 8.89 12.68 14.18 3.23 3.14 5.39 38.09 14.43 69.04 73.15

Total branchedIPL (ng/g)

2.92 0.88 13.24 3.48 1.09 1.03 1.37 ND 4.41 17.79 ND

a ND, not determined.

FIG. 2. Map showing the distribution of abundances of total ar-chaeal core lipids from surface water of the South China Sea. (Mapgenerated with Ocean Data View software.)


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A5 sediment samples with filter samples at water depths near100 m or below showed that the shallow-sediment C-GDGTswere more similar to those in water samples in the same regionthan to those farther away from it (data not shown), suggestinga possible local connection between core-top sedimentGDGTs and those of the planktonic Archaea. The BIT was lessthan 0.2 for both CL and IPL at all water depths (Table 2),indicating minor contributions of terrestrial organic matter inthese locations (17).

TEX86-derived temperatures. (i) SST derived from surfacewater filter samples. Because the filter samples were collectedduring April and May of 2010, satellite-derived sea surfacetemperatures (SST) of April and May 2009 and CTD temper-atures recorded during the sampling period were compared toTEX86-derived temperatures. The satellite and CTD temper-ature maps were consistent in showing the generally higher seasurface temperature in the southern part (below the 17.5°Nline) of the SCS than in the northern part; however, CTDtemperatures to the east of Hainan Island were 2 to 4°C higherthan the satellite temperatures (Fig. 5).

Comparison of satellite sea surface temperatures and thethree calculation methods showed the best match for satelliteSST averaged for April and May of 2009 and the calculationbased on that described by Kim et al. (32) (see Table S1 in thesupplemental material), whereas use of satellite-based meanannual SST showed a poorer correlation (data not shown).Themajority of TEX86 temperatures calculated according to themethod of Kim et al. (32) were lower than satellite tempera-tures (Fig. 6A) or CTD temperatures (Fig. 6B). This was par-ticularly evident in the northern SCS (Fig. 5). On average, thedifference was 3.0 � 2.3°C (n � 57) between satellite seasurface temperatures (averaged for April and May 2009) andTEX86-derived temperatures and 3.4 � 2.9°C (n � 57) be-tween CTD and TEX86 temperatures. The larger differences(e.g., greater than 5.0°C) between satellite sea surface temper-atures and TEX86 values occurred mostly outside the centralbasin and toward the land (e.g., samples 15, 30, 48, 69, 75, 76,and 85) (Fig. 1). The large differences between CTD andTEX86 temperatures also occurred mostly at these stations(data not shown).

FIG. 3. Clustering analysis of relative abundances of glycerol dibiphytanyl glycerol tetraethers (GDGTs) in core lipids of Archaea from surfacewater of the South China Sea. Also plotted are water depths for stations where the surface water samples were collected and total core lipids ofArchaea at each station. D, deep water (1,000 m); S, shallow water (�1,000 m).


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(ii) SST derived from core-top sediments. In most cases theTEX86

H -derived temperatures based on IP-GDGTs were higherthan those based on C-GDGTs (Table 2). In some cases, thedifference between C-GDGT- and IP-GDGT-derived temper-atures could be as large as 18.3°C according to the formula ofSchouten et al. (55) (equation 1). This difference decreasedwhen formulas of Kim et al. (31, 32) (equations 2 and 3) wereused, and the latter formula (equation 3) gave the smallestdifference between the C-GDGT- and IP-GDGT-derived tem-peratures (Table 2).

The TEX86 temperatures determined according to themethod of Kim et al. (32) gave the closest match to the meanannual sea surface temperature from the satellite data. In theCL, the difference between satellite and TEX86 temperatures(32) was less than 1.0°C in all deep-water core-top sedimentsexcept MD05-2902, which had a difference of 1.1°C (Table 2).In core-top sediments from shallower water (A9, A7, and A5),however, the difference was considerably larger (4.3 to 9.2°C),with TEX86 temperatures lower than satellite temperatures(Fig. 7). Overall, the mean difference between mean annualsatellite and TEX86 temperatures was 1.9 � 2.4°C (n � 11),which was much smaller than differences observed for filtersamples (note that the uncertainty of the calibration in use is2.5°C, which is greater than the 1.9°C mean difference ob-served).

In the IPL of the deep-water samples, the difference be-tween satellite and TEX86 temperatures (32) was mostlygreater than 0.5°C, and it was up to 9.3°C in MD05-2896 (Table2). Similar to the case for the CL, the IPL temperatures of theshallow-water core-top sediments gave larger differences from

the satellite values than those of the deeper-water core-topsediments (Table 2).

DISCUSSION

Abundance and distribution of GDGTs. (i) Filter samples.The average concentration of C-GDGTs (0.05 � 0.13 ng/liter;n � 57) for all filter samples (see Table S1 in the supplementalmaterial) was less than 10% of the average concentrations ofC-GDGTs determined in other oceanic water column studies(16, 22, 59, 62, 63). Factors affecting the measured abundanceof C-GDGTs in oceanic waters may include difference in meth-ods of lipid extraction and different relative responses in themass spectrometer, growth stage of the planktonic Archaea,seasonal variation in planktonic archaeal productivity, watercolumn depth, and/or other variables. Huguet et al. (22) com-pared several extraction methods on both a living culture andenvironmental samples. They observed that the living culturehad trace amounts of C-GDGTs, indicating that actively grow-ing cells were composed mostly of IP-GDGTs. Environmentalsamples (including particles from the water column), on theother hand, had considerable amounts of C-GDGTs relative toIP-GDGTs, suggesting that large proportions of environmen-tal lipids were derived from nonliving cells. Those authors alsorecommended using sonication or Soxhlet extraction for stud-ies aiming to determine TEX86-derived temperatures or toquantify the relative abundances of C- versus IP-GDGTs. Ourstudy followed the sonication extraction method recommendedby Huguet et al. (22), and the low concentrations of CL areunlikely to be due to method biases. Although we do not know

FIG. 4. Clustering analysis of relative abundances of glycerol dibiphytanyl glycerol tetraethers (GDGTs) in core lipids of Archaea from core-topsediments of the South China Sea. Also plotted are water depths at which core-top sediment samples were collected and total core lipids of Archaeaat each station.


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the growth stage of the planktonic Archaea in the SCS, esti-mates of lifetimes of planktonic Archaea are on the order ofdays to weeks (24). In reference to what Huguet et al. (21, 23)have observed, the low concentrations of C-GDGTs in ourfilter samples may not represent cells that were all active at thetime of sampling. Another possible explanation for low GDGTconcentrations may be the degradation of these compoundsduring transportation at ambient temperature. However, deg-radation, if any, appears not to have affected the calculation oftemperatures based on the TEX86 formula, which is consistentwith Schouten et al. in that oxic degradation does not affect theTEX86 values within the analytical error (54).

Depth distribution and/or seasonal variation in planktonicArchaea may be better reasons for the low concentrations ofC-GDGTs in the surface water of the SCS. Quantification ofarchaeal biomass using molecular DNA methods has repeat-edly shown that Crenchaeota, which are thought to be themajor producers of GDGTs in the ocean, are at low levels insurface water and increase in relative or absolute abundanceswith depth (see, e.g., references 9, 30, 45, 47, and 65). A studyof archaeal abundance in the SCS showed the same pattern,with surface water (5 m) having about 103 copies of archaeal16S rRNA genes per ng of DNA, whereas at 75 m the archaealabundance was 2 orders of magnitude higher (18). Depth pro-files of archaeal lipids in the Black Sea also showed low GDGTconcentrations in surface water (10 m) and a maximum atabout the 100-m depth, which agrees with the maximumArchaea cell numbers (63). Similarly, in the Gulf of Mexico,GDGTs were detected at depths of 400 m and 869 m but notat 10 m (40). On the other hand, planktonic Archaea also varyin abundance in different seasons, with colder temperaturesfavoring a higher abundance of Archaea in many oceanic re-gimes (14, 16, 48, 65). It is possible that the low concentrationof C-GDGTs in the SCS surface water resulted from samplingin a nonwinter season. This hypothesis has yet to be testedthrough seasonal and vertical sampling of the water columns inthe SCS, which has been planned for the near future.

High abundances of planktonic Archaea are often found inassociation with upwelling and the oxygen minimum zone(OMZ) (1, 10, 33, 36). In the SCS, upwelling commonly occursin regions northwest of Luzon and north of Sunda Shelf inwinter and off the east coast of Vietnam in summer (41). Theabundances of archaeal CL in surface water were indeed en-hanced in these regions, particularly off the east coast of Viet-nam (Fig. 2). However, we did not document whether upwell-ing was occurring during our sampling period, and such acause-effect relation cannot be determined from our data.Also, the high abundance in the region between Hanan Islandand the mainland may be related to upwelling over the wid-ened northern SCS shelf, as indicated by model simulation andlimited observations (15, 29). The OMZ commonly occursbelow the sea surface, and it is unknown how surface (�10-m)archaeal populations may be affected by the OMZ below.

(ii) Sediment samples. The C-GDGTs in the sediment sam-ples (Table 2) are at the lower end of the ranges observed inother marine sediment environments (see Table 4 in reference22). For example, C-GDGTs in the range of 0.09 to 11 �g/gwere reported for the Drammensfjord sediment in Norway (20,23), C-GDGTs in the range of 0.06 to 195 �g/g for the ArabianSea sediment (20), and C-GDGTs in the range of 0.02 to 7.73

TA

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0.8963.48

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29.7130.00

29.0827.97

28.490.03

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�g/g for Atlantic Ocean sediments (19). Lower C-GDGTabundance has been explained as being a result of an enhanceddegradation rate under oxic conditions (19). It is unknownwhether in this study differential degradation contributed tothe lower C-GDGT concentrations in our surface marine sed-iments. On the other hand, the low GDGT concentrations mayreflect the overall oligotrophic conditions of the South ChinaSea (41), which is consistent with the low C-GDGT concen-trations in the surface water and supported by the relativelylow TOC (average � 0.94 � 0.12%, n � 11) in these samples(Table 1) (39).

IP-GDGTs accounted for 6.0 to 36.4% of total GDGTs (Cplus IP). This is consistent with observations reported by oth-ers (20, 38, 42) and suggests that the majority of GDGT lipidsin marine core-top sediments are derived from nonlivingArchaea. The sources of CL and IPL in marine sediments,however, are debated and can come from either in situ pro-duction (3, 38, 39, 42) or possibly relict IPL from the watercolumn (57). In particular, benthic archaeal populations seemto be able to recycle fossil GDGTs from planktonic Archaea(37, 42, 60), which can explain the higher TEX86 temperaturesbased on IPL than on CL (42).

FIG. 5. Maps of satellite-based average sea surface temperatures for the April-May season during which the surface water samples werecollected (left), in situ temperatures determined from CTD (middle), and TEX86-based temperatures of surface water samples according toreference 32. (Maps generated with Ocean Data View software.)

FIG. 6. (A) Correlations between satellite-based sea surface temperatures (from Fig. 5) and TEX86-based temperatures (32). (B) Correlationsbetween CTD in situ temperatures (from Fig. 5) and TEX86-based temperatures (32). In both cases, the correlation is insignificant (P 0.05).


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Our observation of structural changes in CL and IPL (Table2) agrees with a report for other marine sediments (42). How-ever, Liu et al. (42) also showed significant correlations in thering index and in the TEX86-derived temperatures between C-and IP-GDGTs, which allowed them to explain the overallconnections between these two lipid pools with three possibil-ities: (i) the pool of C-GDGTs is strongly influenced by sedi-mentary in situ production and subsequent hydrolysis of IP-GDGTs, (ii) the pool of IP-GDGTs largely representsmolecular fossils derived from planktonic Archaea, and (iii)there is partial recycling by benthic Archaea of fossil C-GDGTsderived from planktonic Archaea (42). Neither our data northose of Liu et al. (42) allow us to draw a conclusion about theexact sources of CL and IPL in the marine sediments. How-ever, the lack of correlations in the ring index and in theTEX86-derived temperatures between C- and IP-GDGTs inour study (data not shown) indicates the presence of othersources of C- and IP-GDGTs in the SCS sediments. Modeling(38, 39, 57) in combination with isotopic measurements ofdifferent intramolecular components of the GDGT molecules(37, 58, 60) and measurements of the metabolic status ofArchaea (22, 24) may be needed to thoroughly evaluate to whatextent the IP-GDGTs represent fossil or living archaeal bio-mass in natural environments.

TEX86-derived temperatures. The development of theTEX86 proxies has significantly advanced our understanding ofpaleoclimate change (12). In the core-top sediments, theTEX86-derived temperatures based on the work of Kim et al.(32) agree with satellite-derived mean annual surface temper-atures except for the shallow (�100-m) water depths, whichshow significantly lower temperatures than satellite values(Fig. 5). A similar discrepancy has been observed on the Italianshelf of the Gulf of Taranto by Leider et al. (35), who attrib-uted the lower TEX86-based temperatures for the near-shoresites to winter sea surface temperatures.

Studies of TEX86 proxies in the water column, however,have resulted in ambiguous conclusions (53, 62). In this study,the satellite-derived as well as measured in situ temperatureswere overall considerably higher than TEX86-based tempera-

tures (Fig. 6). The central basin and the southern part of theSCS, however, show TEX86-derived temperatures matchingthe satellite-derived or measured temperatures (Fig. 5), sug-gesting that planktonic Archaea produce GDGTs in responseto sea surface temperature in these regions (G. Jia [personalcommunication], on the other hand, showed the best matchbetween core-top TEX86-derived temperatures with satellite-derived temperatures at water depths of 30 to 125 m in theSCS). The reasons for the considerably lower TEX86 temper-atures in other parts of the SCS are unknown, and sampling inother seasons is needed to better understand temporal re-sponses of archaeal abundances and community structure tochanges in sea surface temperatures. Changes in nutrients(62), transportation of exogenous cold-water-sourced particles(35), or hydrodynamics of the water column (34, 66) are pos-sible reasons for the discrepancies between TEX86-derived seasurface temperatures and measured temperatures.

Summary. A total of 57 surface water samples and 11 core-top sediment samples from the South China Sea were analyzedfor the abundances of CL and IPL of Archaea. Because of thehigh sensitivity of the LC-MS (detection limit of 0.8 pg), wewere able to measure low concentrations of CL (0.001 to 0.894ng/liter) of Archaea in most of the filter samples. The distribu-tion of the CL was heterogeneous, with high values occurringin regions where upwelling commonly occurs and low valuesoccurring in the southeast area of the SCS. The CL of Archaeain surface marine sediments ranged from 0.11 �g/g to 0.90�g/g, which were at the low end of CL concentrations com-monly observed for other marine sediments and may reflectthe oligotrophic productivity of the SCS. The IPL of Archaearepresented 6 to 36.4% of total lipids (C plus IP), suggestingthat the majority of archaeal lipids in core-top sediments werefossil remains of archaeal cells.

TEX86-derived temperatures were best correlated to satel-lite-based or CTD-determined in situ temperatures when theformula most appropriate for nonpolar oceans was used (32).The TEX86 temperatures for filter samples collected for theApril-May season were better correlated to satellite mean sur-face temperatures for this season than for the mean annual sea

FIG. 7. Annual mean sea surface temperatures (satellite based) and TEX86-derived temperatures for core-top sediment samples versuswater depth.


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surface temperatures, suggesting that planktonic Archaeamight respond to temperature variations at the seasonal scale.Nevertheless, the TEX86 temperatures of the surface waterwere significantly lower than satellite or CTD-derived temper-atures; however, our data do not allow conclusions to be drawnabout the causes of the discrepancies. TEX86 temperaturesfrom surface marine sediments in the open ocean (water depthof 1,000 m) were within 1°C of the mean annual sea surfacetemperatures, suggesting the applicability of TEX86 proxies(32) for paleoclimate studies in at least the central basin of theSouth China Sea. The much lower TEX86 temperatures formarine sediments from depths shallower than 100 m indicatedthat caution must be exercised in interpretation of paleotem-peratures from TEX86 values obtained from the shallow con-tinental shelf of the SCS.

APPENDIX

Figure A1 shows the structures of isoprenoidal and branched glyc-erol dibiphytanyl glycerol tetraether (GDGT) and archaeol.

ACKNOWLEDGMENTS

We appreciate the support of the crews on R/Vs Shiyan No. 3,Haiyang No. 4, Dongfanghong No. 2, and Marion-Dufresne during eachof the cruises conducted for this research. We thank T. Li for collectionof sediment samples during the Marion-Dufresne cruise in 2005. Wethank S. Yang for helping with analyses of total organic carbon andnitrogen, W. Liu for isotopic measurements of TOC, and L. Shao forgrain size determinations.

This research was supported by National Natural Sciences Foundationof China grants 40730844 (M.Z.), 40976022 (L.L.), and 91028005 (C.L.Z.,L.L., and P.W.), Ministry of Science and Technology of China grant2007CB815904 (M.Z., L.L., and P.W.), and the State Key Laboratory ofMarine Geology at Tongji University (L.L., P.W., and C.L.Z.).

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