Paleotemperature variability in central China during the last 13 ka recorded by a novel microbial lipid proxy in the Dajiuhu peat deposit

Abstract

The Asian summer monsoon is a very important climatic component affecting the land ecosystem on the eastern Asian continent. Here we assess microbe-derived lipid biomarker evidence from a well-dated peat core from Dajiuhu to reconstruct paleotemperature changes in central China through the last 13 ka. The branched fatty alcohol ratio BNA₁₅, which is defined as the relative contribution of branched C15 fatty alcohols over their straight-chain homolog, shows a positive correlation with air temperature (R= 0.83, n=11, p<0.001) in an altitude transect at Shennongjia Mountain, central China. This correspondence suggests that the microbial activities associated with branched fatty alcohol synthesis are sensitive to differences in temperature. The BNA₁₅ sequence in the Dajiuhu peat deposit shows a trend similar to the paleotemperature record derived from pollen results over the last 13 ka, further supporting that BNA₁₅ is a sensitive proxy of paleotemperature. Absolute temperatures estimated from BNA₁₅ values of modern surface peats are about 3–4°C lower than the modern annual mean air temperature in the peatland, which may result from the influences of factors other than temperature or from the different microbial communities in the mountain soils used to calibrate the BNA₁₅ acidic peats. Fluctuations in the continuous 13 ka BNA₁₅-derived record of relative temperature change from the Dajiuhu peat core imply that solar activity is the dominant cause for most cold events at multicentennial to submillennial timescales.

Keywords

branched fatty alcohols central China Holocene paleotemperature solar activity

Introduction

Reconstruction of the postglacial history of the East Asian monsoon in China has received great attention in recent decades, using paleoclimate proxies from studies of loess-paleosol sequences, marine and lacustrine sediments, peat deposits, and stalagmites (e.g. Dykoski et al., 2005; Liu and Ding, 1998; Wang et al., 2001; Yancheva et al., 2007; Zhao et al., 2006; Zhou et al., 2004). These records provide a detailed perspective on climate changes in the monsoonal regions of China during the Holocene. In central China, published high-resolution paleoclimate records are mainly based on the calcite oxygen isotopes of cave stalagmites (Cai et al., 2010; Dong J et al., 2010; Hu et al., 2008), but the interpretation of the oxygen isotope variations in Chinese stalagmites remains controversial (Maher and Thompson, 2012; Pausata et al., 2011). Consequently, assessment of new proxies with authentic climatic implications separating from stalagmites or from other archives such as lacustrine sediments and peat deposits is needed. This need is especially important for paleotemperature reconstructions, which have rarely been attempted in central China (Zhu et al., 2008).

Terrestrial ecosystems are known to have responded sensitively to the global changes recorded in geological archives. Because of this behavior, palynological records in sediments indicative of higher plant variations are widely employed as paleoclimatic indicators (e.g. Birks and Birks, 2008; Yu, 2003; Zhao et al., 2009). Whilst a change in vegetation might require a long time period and potentially manifest a delay of one or two centuries (Williams et al., 2002) or even 1000 yr (Zhao et al., 2009) to an abrupt climate change (Hughen et al., 2004; Jennerjahn et al., 2004), microbial ecosystems should give a very sensitive and quasi-annual response (e.g. Dong H et al., 2010; Pancost et al., 2007; Xie et al., 2012; Yao et al., 2008). Previous studies have established several landmark lipid-derived paleotemperature proxies, i.e. U_K³⁷ (Brassell et al., 1986)/ U_K³⁷’ (Prahl and Wakeham, 1987) and TEX₈₆ (Schouten et al., 2002). However, their applications are largely constrained to marine records (Castañeda and Schouten, 2011). To date, only a few microbial lipid paleotemperature proxies specific for terrestrial environments have been developed (Weijers et al., 2007).

The Dajiuhu peatland, located at the north slope of Shennongjia Mountain, central China (Figure 1), is a rare subalpine peatland in the middle latitudes of the Northern Hemisphere. The continuous peat sequence started to deposit more than 13 ka (1 ka= 1000 cal. yr BP) ago (Huang et al., 2012; Li et al., 2012; Zhu et al., 2010). This peat deposit can provide an important opportunity to reconstruct a high-resolution paleoclimate record in central China for the Holocene epoch. Most early studies in this peatland have focused on pollen results (Li et al., 2012; Shi et al., 2008; Zhao et al., 2007; Zhu et al., 2008, 2010). However, our previous study of this peat deposit has shown that lipid biomarkers, especially those from microbes or mediated by microbes, are sensitive to climate changes during the transition from the late deglacial to the early Holocene (Huang et al., 2012). Here we develop a new paleotemperature proxy to assess the temperature variability in central China over the last 13 ka. This new proxy is based on the distribution of short-chain branched fatty alcohols, which are postulated to originate from a still-unidentified bacterial source. We first provide evidence from a soil temperature gradient on Shennongjia Mountain in central China to support the idea that the distribution of branched fatty alcohols is sensitive to the temperature component of climate change. Then we compare the microbial lipid-derived paleotemperature sequence with the pollen record in the same peatland and with other paleotemperature records in nearby regions, to further support that our novel proxy has promising potential to reflect paleotemperature changes in peat deposits.

Figure 1.

Locations of the Dajiuhu Peatland, Shennongjia Mountain, and Dongge Cave in China and generalized trajectories of the Indian and East Asian summer monsoons.

Material and methods

Study site and sampling

Surface soil samples (0–5 cm) were collected from Shennongjia National Nature Reserve in an altitude transect up Shennongjia Mountain, central China. This site is located at the transition between the eastern plains and the western mountainous part of China. A total of 11 soil samples (Table 1) were collected for lipid analyses, covering elevations between 1.1 and 2.9 km above sea level.

Table 1.

Location, altitude and calculated annual mean temperature for soil samples collected on Shennongjia Mountains.

No.	Latitude	Longitude	Altitude (m)	T (°C)^a
1	31°27.094′N	110°31.491′E	1055	12.1
2	31°26.032′N	110°21.569′E	1491	9.5
3	31°26.841N	110°7.098′E	1580	8.9
4	31°27.771′N	110°8.360′E	1684	8.3
5	31°32.124′N	110°19.972′E	1716	8.0
6	31°32.159′N	110°19.982′E	1730	7.9
7	31°29.668′N	110°18.192′E	2156	5.4
8	31°27.518′N	110°13.353′E	2619	2.7
9	31°26.642′N	110°16.391′E	2826	1.5
10	31°26.566′N	110°15.964′E	2859	1.3
11	31°27.094′N	110°16.154′E	2926	0.9

Notes:

The annual mean temperature of each sampling site was calculated according to the function: T=61.657−1.375Φ−0.006H (Zhu et al., 2008), where T is the annual mean temperature, Φ is latitude, H is altitude (m).

Peat samples were collected from the nearby Dajiuhu peatland (31°28′ N, 110°0′ E; 1700 m above sea level) on the north slope of Shennongjia Mountain. The samples for branched fatty alcohol analysis were selected at 1 cm intervals from the surface to 160 cm and at 3 cm intervals from 160 to 260 cm from a core that was collected in 2005. The chronostratigraphy for this core is based on 14 AMS ¹⁴C dates of bulk plant residues (for details see Huang et al., 2012). In addition, two surface peat samples (0–2 cm) were collected from Dajiuhu in September 2009 to compare the distributions of solvent-extractable branched fatty alcohols and those released from saponification of wax esters.

Lipid extraction and fractionation

The extraction and fractionation procedures for soil and peat core samples used here have been described by Huang et al. (2012). To summarize, lipids were ultrasonically extracted from freeze-dried soil samples with chloroform and then fractionated into aliphatic, aromatic and polar fractions using silica gel column chromatography with hexane, benzene and methanol, respectively, as elution solvents. 5β(H)-cholane and pregnanol were used as internal standards for the hexane and methanol eluted fractions, respectively. The polar fraction of total lipid extracts was saponified by heating (2 h, 70°C) with 2 ml 1 M KOH/methanol, to hydrolyze esters and then separated into acidic and neutral fractions. The neutral fraction was reacted with bis(trimethylsilyl)trifluoroacetamide (BSTFA) to produce trimethylsilyl ethers of fatty alcohols. For peat samples, the polar fraction containing branched fatty acids and alcohols was sequentially reacted with BF₃-methanol (14%, v/v) and BSTFA to form fatty acid methyl esters and trimethylsilyl ethers of fatty alcohols.

The surface peats were treated nearly the same as the peat core samples. An important difference is that after fractionation using silica gel column chromatography, one aliquot of the polar fraction was saponified as in the soil samples. Another aliquot of the polar fraction was not treated with the saponification procedure. The fatty alcohol fraction of both treatments was reacted with BSTFA before gas chromatography-mass spectrometry (GC-MS) analyses.

Instrumental analyses

GC-MS analyses were conducted on a Hewlett Packard 6890 gas chromatograph interfaced with a Hewlett Packard 5973 mass selective detector. The chromatograph was equipped with a DB-5 MS capillary column (30 m × 0.25 mm, film thickness 0.25 μm). Samples were injected in a splitless mode (1 μl). The oven temperature was programmed as follows: initial temperature at 70°C for 1 min, and then increased to 200°C at 10°C/min, and finally increased to 300°C at 3°C/min and kept isothermal for 10 min. Helium was used as the carrier gas at a constant flow of 1 ml/min. The ionization energy of the mass spectrometer was set at 70 eV; the scan ranged from 50 to 550 Dalton. Compound identifications were assigned on the basis of mass spectra and the relative retention times from the literature (Cranwell, 1980; Mudge and Norris, 1997; Treignier et al., 2006).

Results and discussion

Distributions of branched fatty alcohols in peat samples

Short chain branched fatty acids and fatty alcohols occur in all peat samples and are dominated by the C15 and C17 iso- and anteiso-isomers (Figure 2). Branched alkanes are absent or below the detection limit in these peat samples. Because branched C17 fatty acids and fatty alcohols are quite low in many of the peat samples, we focus on the more abundant branched C15 fatty acids and fatty alcohols in our discussion and interpretation.

Figure 2.

The m/z 103 mass chromatogram of fatty alchols (as trimethylsilyl ethers) and m/z 74 mass chromatogram of fatty acids (as methyl esters) in the Dajiuhu peat deposit. The arabic numbers on the peaks refer to the carbon chain lengths. i and a refer to iso- and anteiso-isomers.

Branched fatty acids and fatty alcohols are distinctive metabolic products of microbes (Kaneda, 1991; Parkes, 1987; Treignier et al., 2006). Thus the presence of these biomarker molecules can act as the recorders of microbial activities, and changes in their abundance can be indicators of changes in the environmental conditions that affect the microbes. However, the large susceptibilities to degradation of short chain fatty acids prevent them from being robust recorders of microbial activities in long time-sequences (Meyers, 2003; Xie et al., 2004). Therefore, to assess temperature-related variations in microbial activities over the Holocene, here we create a new branched fatty alcohol ratio BNA₁₅, defined as following:

{BNA}_{15} = ([i - C_{15}] + [a - C_{15}]) / [n - C_{15}]

(1)

The values of BNA₁₅ vary between 0.53 and 8.84, averaging 3.10 over the entire peat sequence (Figure 3). In addition, BNA₁₅ does not show a progressive decreasing trend, revealing that this ratio is relatively stable against degradation over the last 13 ka and hence having the potential to record original environmental information.

Figure 3.

Variations of BNA₁₅ in the Dajiuhu peat sequence over the last 13 ka.

For the soil samples collected from Shennongjia Mountain altitude transect, relatively high amounts of branched fatty alcohols can be detected only after saponification. The alkanol compositions of two surface peat samples collected from Dajiuhu were compared before and after saponification (Figure 4). The saponification doubles the content of C₁₅ iso-fatty alcohol and increases C₁₅ anteiso-fatty alcohol by 50%. Important to this study, the saponification treatment yields a value of BNA₁₅ very similar to the non-saponification treatment (Peat-1 0.92 vs. 0.96; Peat-2 1.22 vs. 1.22; Figure 4). Although we do not yet know the specific precursor of branched fatty alcohols or their physiological function in microbial cells, the increased yields from the saponification experiments suggest that the branched alcohols in the soil and peat samples largely originate from branched wax esters with branched fatty alcohol moieties.

Figure 4.

Comparisons of distributions of fatty alcohols in the surface peat samples obtained by solvent extraction with and without saponification of the samples.

Climatic significance of the branched fatty alcohol ratio

The potential climatic significance of the variations in the branched fatty alcohol ratio BNA₁₅ can be assessed with the suite of soil samples collected from the altitude transect on Shennongjia Mountain. The annual mean temperature of each sampling site (Table 1) was calculated according to the function between temperature and altitude and latitude established by Zhu et al. (2008). The BNA₁₅ of the soil samples shows a positive correlation with air temperature (R= 0.83, n=11, p<0.001; Figure 5). The good correlation between BNA₁₅ and temperature suggests that microbial activities are greater in warmer conditions, which is consistent with the finding that higher bacterial abundance and diversity normally occur in warmer climates (Almagro et al., 2009; Dong H et al., 2010; Fang and Moncrieff, 2001). Hydrological conditions, especially the relative humidity, can also affect bacterial activity by lowering intracellular water potential in drier settings (Schimel et al., 1999). At Shennongjia Mountain, the relative humidity is nearly constant (c. 80%) at different altitudes (Luo et al., 2011). Consequently, even though precipitation increases with altitude at Shennongjia Mountain (Luo et al., 2011), we postulate that temperature exerts a more important effect than precipitation on the level of the microbial activities that lead to branched fatty alcohol synthesis in the perennially moist soils of Shennongjia Mountain.

Figure 5.

Correlation between BNA₁₅ and air temperature for soil samples collected from an altitude transect on Shennongjia Mountain.

Despite the empirical evidence for their correspondence, the actual mechanism that links microbial fatty alcohol distributions and climate change remains unclear, partially because of the quite limited reports of their occurrence in sediments and microbes. Although wax esters with branched fatty alcohol moieties have been detected in green nonsulfur-like bacterial mats from hot springs (Jahnke et al., 2004; Schouten et al., 2009), the dramatic differences between hot springs and acidic peats make it hard to consider the two environments as analogous. However, one possibility is that branched wax esters act as a stabilizer for cell membranes at elevated temperatures, as deduced for green sulfur bacteria and green nonsulfur-like bacteria (Sørensen et al., 2008). Certainly, this hypothesis needs further investigation.

If the BNA₁₅ values of both peat and soil samples in the Shennongjia region fit the same regression function:

T = {BNA}_{15} \times 0.88 + 0.52

(2)

then the air temperatures (T) inferred from the BNA₁₅ of the two surface peat samples are 1.3–1.6°C, which are somewhat lower than the present annual mean temperature in Dajiuhu (7.2°C; He, 2007). The BNA₁₅ of the topmost sample (183 yr BP) of the peat core yields a temperature of 3.1°C, which is also lower than the modern instrumental record of temperature. This temperature underestimation may result from the influence from other environmental factors. The most obvious difference between the soil and peat samples in the Shennongjia region is the water chemistry. The water bathing the peat samples is more acidic than the water in the mountain soils, a difference that can modify the relative importance of branched fatty alcohol synthesizing microbes in the whole microbial community at each location. Previous studies revealed that pH is a very important factor in controlling the microbial community in soils (Bååth and Anderson, 2007; Griffiths et al., 2011). Another possible difference is that the types of plants whose residues provide substrate for the microbial communities in peat and soils are not the same. The microbial communities therefore may not be the same. Consequently, future studies should develop a transfer function based upon peat samples with similar water chemistries to reconstruct absolute paleotemperatures in peat sequences.

Despite these differences in absolute temperatures, the record of BNA₁₅ inferred paleotemperature changes in the Dajiuhu peat core has a similar trend with pollen derived temperature sequence from the same peatland (Zhu et al., 2008). Both records show a sharp cooling event during 12.4–11.2 ka, a gradual warming towards the Holocene, and finally a cooling trend in the late Holocene (Figure 6). These shifts broadly follow the changes of solar insolation in the Northern Hemisphere during the past 13 ka (Figure 6; Berger and Loutre, 1991). In addition, our BNA₁₅ record is also consistent with GDGT derived paleotemperature records in the nearby loess sections (Gao et al., 2012; Peterse et al., 2011). As mentioned above, the temperatures inferred from our BNA₁₅ record are generally 3–4°C lower than the pollen derived temperature record. For example, our BNA₁₅ record shows a quite low temperature during the Younger Dryas (about 2°C), whereas the pollen record indicates a temperature near 5°C. Over the last 11 ka, our BNA₁₅ record exhibits a fluctuation of temperature between 8.3 and 1.0°C (Figure 6), while the pollen record shows a fluctuation of less than 3°C (Zhu et al., 2008).

Figure 6.

Comparisons of BNA₁₅ with the pollen derived paleotemperature record in the Dajiuhu peatland (Zhu et al., 2008), the solar insolation changes in the Northern Hemisphere (Berger and Loutre, 1991), the δ¹⁸O sequence at Dongge Cave (Dykoski et al., 2005), and the Ti content in the Cariaco Basin paleoclimate record (Haug et al., 2001) during the last 13 ka.

At the millennial timescale, the BNA₁₅ profile in the Dajiuhu peat sequence shows a good correlation with the oxygen isotope Holocene paleoclimate reconstruction from the D4 stalagmite from Dongge Cave (R= −0.64, p<0.001; Figure 6). The oxygen isotope composition of stalagmites is widely interpreted as a proxy of monsoon intensity (e.g. Dykoski et al., 2005; Wang et al., 2005). In addition, the Dajiuhu BNA₁₅ sequence exhibits an obvious positive correlation with the Ti content in the Cariaco Basin (R= 0.60, p<0.001), which is an indicator of the postglacial shifts in the mean position of the intertropical convergence zone (ITCZ; Haug et al., 2001). These agreements further support that our branched fatty alcohol ratio has the promising potential to track paleoclimate changes during the Holocene epoch.

At the multicentennial to submillennial timescale, the general trend of BNA₁₅ is punctuated by some low value intervals (Figure 6). Some of these intervals are, within dating error, consistent with the weak monsoon events documented in Dongge Cave (Dykoski et al., 2005; Wang et al., 2005). Seven of these intervals are in phase with the Bond cold events documented in the North Atlantic (Bond et al., 2001). When comparing with the archive of solar activity, inferred from residual Δ¹⁴C data (Reimer et al., 2004), cold intervals normally occur during intervals with low solar activity. These agreements suggest that solar activity is an important cause of the monsoon variability at multicentennial to submillennial timescales, as previous studies have suggested (Marchitto et al., 2010; Selvaraj et al., 2007; Wang et al., 2005).

Conclusions

This study provides novel lipid biomarker evidence to reconstruct paleotemperatures in central China during the last 13 ka. Prominent amounts of branched fatty alcohols were identified in samples of the Dajiuhu peat deposit. These branched fatty alcohols are dominated by isomers of C₁₅ and C₁₇, likely originating from microbes inhabiting the acidic peat. We introduce a new branched fatty alcohol ratio BNA₁₅ (branched/normal fatty alcohols with a 15-carbon chain length) to reflect the variations of microbes synthesizing the branched iso and anteiso fatty alcohols in the Dajiuhu peat sequence.

Soil samples along an altitude gradient were collected from the nearby Shennongjia Mountain to assess how BNA₁₅ responds to different climate settings. Results show that BNA₁₅ positively correlates with air temperature, with higher values occurring in warmer low altitude sites. This phenomenon suggests that air temperature is a major factor to create the differences of BNA₁₅ in soils from different settings. The BNA₁₅ sequence in the Dajiuhu peat deposit shows a trend similar to the paleotemperature record derived from pollen results, further supporting the BNA₁₅ as a sensitive proxy of paleotemperature. An unresolved issue with the BNA₁₅ proxy is that it consistently underestimates the environmental air temperature. This underestimation may result from the influence of environmental factors other than temperature. One possibility is that the microbial communities in soil and acidic peat may respond differently to climate changes.

Footnotes

Acknowledgements

Huan Yang, Dr Guoqiao Xiao and Dr Yang Pu are thanked for their help during the preparation of this paper. We especially appreciate the constructive comments of the associate editor and the two anonymous reviewers that helped us to improve this contribution.

Funding

This work was supported by 973 program (2011CB808800), NSFC (grant 40930210, 41102215, 41130207, 30900079), and the fundamental research funds for the central universities, China University of Geosciences (CUG120103, CUG120401).

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