CBT palaeotemperatures from an equatorial African lake

Quaternary Science Reviews 50 (2012) 43e54

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Distribution of tetraether lipids in the 25-ka sedimentary record of Lake Challa: extracting reliable TEX86 and MBT/CBT palaeotemperatures from an equatorial African lake Jaap S. Sinninghe Damsté a, b, *, Jort Ossebaar a, Stefan Schouten a, b, Dirk Verschuren c a b c

Utrecht University, Faculty of Geosciences, P.O. Box 80.021, 3508 TA Utrecht, The Netherlands NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Organic Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands Limnology Unit, Department of Biology, Ghent University, B-9000 Gent, Belgium

a r t i c l e i n f o

a b s t r a c t

Article history: Received 3 February 2012 Received in revised form 27 June 2012 Accepted 2 July 2012 Available online 9 August 2012

The distribution of isoprenoid and branched glycerol dialkyl glycerol tetraether (GDGT) lipids was studied in the sedimentary record of Lake Challa, a permanently stratified, partly anoxic crater lake on the southeastern slope of Mt. Kilimanjaro (Kenya/Tanzania), to examine if the GDGTs could be used to reconstruct past variation in regional temperature. The study material comprised 230 samples from a continuous sediment sequence spanning the last 25 ka with excellent age control based on highresolution AMS 14C dating. The distribution of GDGTs showed large variation through time. In some time intervals (i.e., from 20.4 to 15.9 ka BP and during the Younger Dryas, 12.9e11.7 ka BP) crenarchaeol was the most abundant GDGT, whereas at other times (i.e., during the Early Holocene) branched GDGTs and GDGT-0 were the major GDGT constituents. In some intervals of the sequence the relative abundance of GDGT-0 and GDGT-2 was too high to be derived exclusively from lacustrine Thaumarchaeota, suggesting a sizable contribution from methanogens and other archaea. This severely complicated application of TEX86 palaeothermometry in this lake, and limited reliable reconstruction of lake water temperature to the time interval 25e13 ka BP, i.e. the Last Glacial Maximum and the period of postglacial warming. The TEX86-inferred timing of this warming is similar to that recorded previously in two of the large African rift lakes, while its magnitude is slightly or much higher than that recorded at these other sites, depending on which lake-based TEX86 calibration is used. Application of calibration models based on distributions of branched GDGTs developed for lakes inferred temperatures of 15e18
C for the Last Glacial Maximum and 19e22
C for the Holocene. However, the MBT/CBT palaeothermometer reconstructs temperatures as low as 12
C for a Lateglacial period centred on 15 ka BP. Variation in down-core values of the BIT index are mainly determined by the varying production rate of crenarchaeol relative to in-situ produced branched GDGTs. The apparent relationship of the BIT index with climatic moisture balance can be explained either by the direct influence of lake level and wind strength on nutrient recycling, or by influx of soil nutrients promoting aquatic productivity and nitrification. This study shows that GDGTs can aid in obtaining climatic information from lake records but that the obtained data should be interpreted with care. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Glycerol dialkyl glycerol tetraether Lake sediments Archaea Bacteria TEX86 MBT CBT Holocene Younger Dryas LGM

1. Introduction Abbreviations: BIT, Branched and Isoprenoid Tetraether; CBT, Cyclisation ratio of Branched Tetraethers; GDGT, Glycerol Dialkyl Glycerol Tetraether; HPLC/APCI-MS, High-Performance Liquid Chromatography/Atmospheric-Pressure Chemical Ionization/Mass Spectrometry; LGM, Last Glacial Maximum; MAAT, Mean Annual Air Temperature; MBT, Methylation index of Branched Tetraethers; TEX86, TetraEther indeX of 86 carbon atoms. * Corresponding author. NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Organic Biogeochemistry, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands. Fax: þ31 222 319674. E-mail address: [email protected] (J.S. Sinninghe Damsté). 0277-3791/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.quascirev.2012.07.001

Lake-sediment records often are excellent archives of past climate change, especially for the Quaternary period. Recently, glycerol dialkyl glycerol tetraethers (GDGTs), which are lipids comprising the cell membrane of archaea and certain bacteria, have become a highly versatile tool in palaeolimnology. The temperature-dependent relative number of cyclopentane moieties in GDGT molecules derived from aquatic Thaumarchaeota, formerly

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known as mesophilic or Group 1 Crenarchaeota (Brochier-Armanet et al., 2008; Spang et al., 2010) allowed Schouten et al. (2002) to develop a palaeothermometer based on the TEX86 (TetraEther indeX of 86 carbon atoms), which quantifies the relative abundance of these GDGTs. Analysis of a wide geographical range of surfacesediment samples from marine (Kim et al., 2008) and lacustrine (Blaga et al., 2009; Powers et al., 2010) settings showed that the TEX86 is linearly correlated with sea or lake surface temperature. Using the TEX86 lake calibration, Powers et al. (2005), Woltering et al. (2011) and Tierney et al. (2008, 2010a) reconstructed mean annual LST from the last glacial period to the present for two large rift lakes in East Africa, Lake Malawi (9
e14
S) and Lake Tanganyika (3
e8
S). TEX86 palaeothermometry has, however, been shown not to be applicable to every lake system. Detailed study of surface sediments from large sets of lakes on different continents (Blaga et al., 2009; Powers et al., 2010) showed that lakes may often receive a high amount of archaeal isoprenoid GDGTs derived from soils in the surrounding catchment, which interfere with the fingerprint of GDGTs produced in situ in the lake by the Thaumarchaeota. These conditions can be recognized by looking at a specific GDGT ratio, the so-called Branched and Isoprenoid Tetraether (BIT) index (Hopmans et al., 2004), which is based on the idea that branched GDGTs are primarily derived from bacteria inhabiting terrestrial soils (Weijers et al., 2006b). A second potential problem in the application of TEX86 palaeothermometry is interference from methanogenic archaea. Some of these archaea produce predominantly GDGT-0 (structure I in Fig. 1), which is not used in the TEX86, but also smaller amounts of GDGTs with cyclopentane moieties (i.e., structures II, III and IV), which interfere with the distribution of Thaumarchaeotal GDGTs, and hence yield unreliable TEX86 temperature estimates (Blaga et al., 2009; Bechtel et al., 2010). A second organic geochemical tool with applications in palaeoclimatology is based on bacteria-derived branched GDGTs, which have been identified in peats, soils and lake sediments (Weijers et al., 2006b). These GDGTs (Weijers et al., 2006a; Sinninghe Damsté et al., 2011a) comprise three basic structural groups, namely GDGTs containing 4, 5, or 6 methyl substituents on the nalkyl chain (structures VI, VII and VIII, respectively). A study of

branched GDGTs in soils revealed that their distribution contains palaeoenvironmental information, namely the temperature and pH of the soil (Weijers et al., 2007b). The degree of cyclisation of the branched GDGTs, expressed in the Cyclisation ratio of Branched Tetraethers (CBT) index, correlated well with soil pH, whereas the degree of methylation, expressed in the Methylation index of Branched Tetraethers (MBT), depends on both soil pH and Mean Annual Air Temperature (MAAT) (Weijers et al., 2007b). With these empirical relationships it was possible to derive palaeoenvironmental inferences from the distribution of fossil branched GDGTs (e.g., Weijers et al., 2007a). Lake sediments contain variable but often high amounts of branched GDGTs, and it was assumed that they entered the lakes by soil erosion and its transport by rivers and run-off (Blaga et al., 2009; Powers et al., 2010). In this way, lake sediments could archive soil-derived branched GDGTs and in principle be used to reconstruct the MAAT and pH of soil in the lake’s catchment. However, an increasing number of follow-up studies (Sinninghe Damsté et al., 2009; Tierney and Russell, 2009; Bechtel et al., 2010; Blaga et al., 2010; Tierney et al., 2010b; Tyler et al., 2010; Zink et al., 2010; Loomis et al., 2011; Pearson et al., 2011; Sun et al., 2011; Tierney et al., 2012) have found that the distribution of branched GDGTs in catchment soils and recently deposited lake sediment itself are often quite different, leading to inferred MAAT values that are up to ca 10
C colder than actually observed in those catchments. This pointed to in-situ production of branched GDGTs either in the water column or in the bottom sediments of lakes. Recently, Tierney et al. (2010b) and Pearson et al. (2011) have produced branched GDGT calibrations based on lake sediments, which are substantially different from the original calibration based on soils (Weijers et al., 2007b). Previously we studied the present-day processes affecting GDGT distributions in and around Lake Challa, a permanently stratified crater lake near Mt. Kilimanjaro in equatorial East Africa (Sinninghe Damsté et al., 2009). A time series of monthly sediment-trap samples covering one complete annual cycle revealed that crenarchaeol and related isoprenoid GDGTs were predominantly produced in January and February, following the locally prominent short rain season (NovembereDecember). The TEX86-inferred temperature derived from sedimenting particles collected at 35 m

Fig. 1. Structures of isoprenoid and branched GDGTs discussed in the text. The regio-isomer of crenarchaeol (V0 ) is not shown but possesses an anti-parallel configuration of the two glycerol moieties (see Sinninghe Damsté et al., 2002).

J.S. Sinninghe Damsté et al. / Quaternary Science Reviews 50 (2012) 43e54

water depth corresponded well with observed lake surface-water temperature at this time of largest crenarchaeol flux. Molecular ecological analysis showed that Group 1.1a and 1.1b Thaumarchaeota were the most likely source organisms of these GDGTs. It was inferred that GDGT-0 in the lake sediments did not only originate from lake surface-dwelling Thaumarchaeota but mainly from archaea inhabiting the deeper, anoxic part of the water column based upon analysis of GDGTs in suspended particulate matter in the anoxic water column of the lake. The main flux of branched GDGTs to the sediment was during the short rain season (NovembereDecember) and thus most probably derived from eroded catchment soils in surface run-off. However, a mismatch in the distribution of branched GDGTs in profundal surface sediments with those of catchment soils indicated that a contribution from insitu production of branched GDGTs (i.e., within the lake sediment or the water column) could not be excluded. Here we study the distribution of both isoprenoid and branched GDGTs in the sedimentary record of Lake Challa. We analysed the GDGT composition of 230 sediment samples from a 20.60-m long, continuous and extremely well-dated sediment sequence covering the last 25,000 years. Following our previous reporting of the BITindex data (Verschuren et al., 2009), we here discuss the sources of the different GDGTs and the potential and pitfalls of the TEX86 and MBT/CBT methods for reconstructing local palaeotemperature variations.

2. Materials and methods 2.1. Study site Lake Challa (3
190 S, 37
420 E) is a relatively large and deep Crater Lake situated at an elevation of ca 880 m on the lower south-east slope of Mt. Kilimanjaro. It has a surface area of ca 4.5 km2 and a maximum depth of ca 95 m. The water budget of the lake is determined by sub-surface in- and outflow, precipitation on the lake surface, and evaporation. The sub-surface inflow derives most probably from percolation of precipitation falling predominantly in the montane forest zone of Mt. Kilimanjaro, at 1800e2800 m elevation. Steep crater walls, which reach up to 170 m above the lake surface, confine the catchment of the lake and limit surface inflow to direct run-off. Seasonal rainfall patterns are mainly determined by twice-yearly passing of the Inter-Tropical Convergence Zone (ITCZ) over the region, resulting in a “long rain” (MarcheMay) and “short rain” (OctobereDecember) season. Air temperatures in this region just south of the equator are lowest during northern hemisphere summer (JuneeAugust) and highest during northern hemisphere winter (NovembereMarch). Consequently, maximum surface-water warming (to w27.5
C) occurs in FebruaryeMarch, and deep mixing of the water column occurs between June and September when surface temperature is w23
C. Deep seasonal mixing extends down to 45e60 m water depth, whereas daily wind-driven mixing is limited to 15e20 m depth year-round. A constant temperature of 22.2
C and complete anoxia at greater depths indicate that the lower water column is permanently stratified, or at most mixes with a frequency on the order of once in a decade or less.

MBT ¼

45

2.2. Core sampling A seismic-reflection survey revealed the typical crater basin morphology of Lake Challa, with steep underwater slopes to w60e70 m depth, a gently dipping basin-floor periphery and flat central lake bottom (Moernaut et al., 2010). In 2003 and 2005, gravity cores with intact sedimentewater interface, a miniKullenberg piston core of 2.6 m length and three parallel UWITEC hammer-driven piston cores of 22 m were recovered from the same mid-lake location (Verschuren et al., 2009). Together these comprise a 21.65-m long composite profile of mostly finely laminated organic muds rich in diatom silica. Textural analysis and XRF elemental scanning identified five turbidites (42, 36, 5, 6 and 14 cm thick) consisting largely of re-deposited crater slope material. Excision of these sections yielded a 20.60-m long sequence of continuous offshore lacustrine sedimentation. The age-depth model of the composite core is based on a smoothed spline through INTCAL04-calibrated AMS 14C ages of 164 bulk organic carbon samples as described elsewhere (Blaauw et al., 2011). This study concerns 230 4-cm thick sediment intervals extracted every 4 cm for the uppermost 3 m and then every 12 cm for the remaining section of the profile. 2.3. GDGT analysis Sediments were analysed as described by Sinninghe Damsté et al. (2009). Briefly, 1e3 g dry weight of freeze-dried and homogenized sediment was extracted using the DionexÔ accelerated solvent extraction technique. The polar fraction of the extract was analysed by high-performance liquid chromatography/ atmospheric-pressure chemical ionization/mass spectrometry (HPLC/APCI-MS) on an Agilent 1100 HPLC connected to an MSD SL mass detector according to Schouten et al. (2007). GDGTs were detected by Single Ion Monitoring (SIM) of their [M þ H]þ ions (dwell time 234 m s for each ion) and quantified by integration of peak areas. All samples were run twice. In one LC/MS run the ions m/z 1302, 1300, 1298, 1296, 1292, 1050, 1036, and 1022 were measured and these runs were used to calculate the relative abundances of the major GDGTs, TEX86, and BIT index. In a second LC/MS run the ions m/z 1292, 1050, 1048, 1046, 1036, 1034, 1032, 1022, 1020 and 1018 were measured and used to calculate the relative abundances of all branched GDGTs, MBT, CBT and BIT index. Fifteen samples were run in duplicate for measurement of TEX86; their average difference in TEX86 values is 0.005  0.003 (stdev). All samples were run in duplicate for determination of BIT index; their average difference in BIT-index values is 0.015  0.011 (stdev). Indices based on the distribution of GDGTs were calculated as follows:

TEX86 ¼

BIT ¼

ð½III þ ½IV þ ½V0 Þ ð½II þ ½III þ ½IVÞ þ ½V0 Þ

ð½VI þ ½VII þ ½VIIIÞ ð½V þ ½VI þ ½VII þ ½VIIIÞ

ð½VI þ ½VIb þ ½VIcÞ ð½VI þ ½VIb þ ½VIcÞ þ ð½VII þ ½VIIb þ ½VIIcÞ þ ð½VIII þ ½VIIIb þ ½VIIIcÞ

(1)

(2)

(3)

46

CBT ¼ Log

J.S. Sinninghe Damsté et al. / Quaternary Science Reviews 50 (2012) 43e54

  ½VIb þ ½VIIb ½VI þ ½VII

(4)

with Roman numerals corresponding to the GDGT structures drawn in Fig. 1. TEX86-inferred lake-surface temperature (LST) was calculated using the calibration equations of Powers et al. (2010) and Tierney et al. (2010a), respectively:

LST ¼ 55:2*TEX86  14:0

(5)

LST ¼ 38:9*TEX86  3:5

(6)

MBT- and CBT-inferred mean annual air temperatures (MAAT) were calculated using the African lake calibrations of Tierney et al. (2010b):

MAAT ¼ 11:8 þ 32:5*MBT  9:3*CBT

(7)

In addition we used the recent calibration of Pearson et al. (2011) to calculate MAAT:

MAAT ¼ 20:9 þ 98:1*FVIb  12:0*FVII  20:5*FVII

(8)

where F is the fractional abundance of a specific branched GDGT relative to the total branched GDGTs. 3. Results The ca 230 studied horizons of the Challa sediment sequence showed a wide variety in GDGT composition. This is evident from the large variation in the average relative abundance of major GDGTs, i.e. GDGT-0 (I), crenarchaeol (V), and the three branched GDGTs without a cyclopentane moiety (VI, VII, and VIII) over selected time intervals (Fig. 2). The other, minor isoprenoid GDGTs (GDGT-1, II; GDGT-2, III; GDGT-3, IV) and the crenarchaeol regioisomer (V0 ) individually represent between 0.1 and 7.3% of the total GDGTs (Fig. 2). The branched GDGTs VIa and VIIa are present in relative amounts of between 2.3 and 4.1% of the total GDGTs, whereas the branched GDGTs (VIb, VIb, VIIa, and VIIb) are trace components (<0.4%) only (Fig. 2). The distributions of the major GDGTs show distinct variations with time as shown in the ternary diagram (Fig. 3). In most of the Holocene sediments (9.6e0 ka BP; time slice A) GDGT-0 and the branched GDGTs are the major components (Figs. 2a and 3). Crenarchaeol represents 19% of the total GDGTs on average, with an exception for two short time intervals discussed further below. In

Fig. 2. Bar plots showing the average distribution (with standard deviation) for GDGTs IeVIII in Lake Challa sediments for selected time slices. The white bar represents GDGT-0, the black bars the other isoprenoid GDGTs (IIeV), and the grey bars all branched GDGTs (VIeVIII). The distributions were obtained by quantification of all of the GDGTs and normalizing the relative abundance of each GDGT on the total sum of GDGTs. Error bars indicate the standard deviation.

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47

high variability is also evident from the large fluctuations in the BIT index and %GDGT-0 abundance (Fig. 4). 4. Discussion 4.1. The BIT index record

Fig. 3. Ternary diagram showing the distribution of the major GDGTs, i.e. GDGT-0, crenarchaeol (including the crenarchaeol regio-isomer), and the summed branched GDGTs in 0e25 ka old sediments of Lake Challa. Colours indicate sediment samples from different time slices (see text). In case of the sediments from the Younger Dryas a line connects the stratigraphically related data points; this shows that there is a gradual evolution from a GDGT composition that falls in the cloud of data points from the Holocene towards that of sediments from the LGM.

the earliest Holocene (11.6e9.8 ka BP; time slice B) crenarchaeol is far less dominant and only represents 2.4% on average of the total GDGTs (Fig. 2b). This is also evident from the relatively high values of the BIT index (0.94 on average) and the abundance of GDGT-0 relative to crenarchaeol (%GDGT-0 ¼ [I]/([I]þ[V])*100), while MBT and CBT ratios are not substantially different from those in time slice A (Fig. 4cef). The Younger Dryas (13.1e11.7 ka BP; time slice C) is a period of marked change in GDGT distribution, as it is in other biogeochemical records from Lake Challa (Tierney et al., 2011; Sinninghe Damsté et al., 2011b). The five sediment horizons analysed from the middle of this time interval (12.8e12.2 ka BP) show an average GDGT distribution that is dominated by crenarchaeol (39%) and also contains higher amounts of the other isoprenoid GDGTs (Fig. 2c). This is also evident from the much reduced BIT index and %GDGT-0 values (Fig. 4c and d). The marked change in GDGT distribution between the peak Younger Dryas and the earliest Holocene (time slice B) is gradual, as is illustrated by the line connecting adjacent sediment horizons of time slice C in the ternary diagram (Fig. 3) and the BIT index and %GDGT-0 plots (Fig. 4c and d). The Lateglacial period just before the Younger Dryas (15.7e12.9 ka BP; time slice D) shows a quite variable GDGT distribution (Fig. 2d; note the large standard deviation of especially crenarchaeol) that is similar to that of most of the Holocene (Fig. 2a) except for the branched GDGTs that show a different pattern (see the distinct MBT and CBT values in Fig. 4e and f). Sediments from the period between 20.4 and 15.9 ka BP (late LGM and early Lateglacial period; time slice E) show the most pronounced dominance of crenarchaeol of all time slices, where it represents on average 43% of all GDGTs (Fig. 2e). This results in low values of the BIT index and %GDGT-0 abundance for this interval (Fig. 4c and d). The GDGT composition of this interval is rather similar to that of peak Younger Dryas sediments (Fig. 2c) except that branched GDGT VIII is more abundant relative to the other branched GDGTs. GDGT distributions in sediments from time slice F (24.9e20.5 ka BP), thus largely coinciding with the LGM (26.5e19.0 ka; Clark et al., 2009) are much more variable (Fig. 2f; note the large standard deviations) and are much less dominated by crenarchaeol than the early Lateglacial sediments of time slice E. The

We have previously used the BIT index record of Lake Challa (Fig. 4d) as a recorder of rainfall intensity in this area (Verschuren et al., 2009) under the assumption that the branched GDGTs in the lake sediments were derived from branched GDGTs in soils from within the lake catchment. Increased rainfall would erode and flush more soil organic matter into the lake, resulting in a higher BIT index. This interpretation fits well with the record of past lake-level fluctuation in Lake Challa inferred from seismic-reflection stratigraphy (Moernaut et al., 2010) and the assembled existing climate data for equatorial Africa: relatively wet conditions going into the LGM, a dry period 20e15 ka BP and subsequently an increasingly wet climate, culminating in the very wet Early Holocene (Verschuren et al., 2009). This trend of increasing precipitation was interrupted by the regionally dry Younger Dryas period (Gasse et al., 2008), which is characterized by substantially lower BIT values (Fig. 4d). Also, the rapid and strong increase in BIT index around 11.7 ka BP coincides, within dating uncertainty, with the end of the YD recorded in Greenland ice (Severinghaus et al., 1998) and the resumption of a strong monsoon circulation, and consequently wetter conditions, at that time (Talbot et al., 2007). Finally, it coincides with the age of the oldest ice on Mt. Kilimanjaro (Thompson et al., 2002), supporting the interpretation of the BIT record as a proxy for precipitation since Mt. Kilimanjaro’s ice-cap dynamics are predominantly determined by precipitation (e.g., Kaser et al., 2004). 4.1.1. Potential in-situ production of branched GDGTs In our study of the present-day processes governing the distribution of GDGTs in and around Lake Challa (Sinninghe Damsté et al., 2009), we showed that the major downward flux of branched GDGTs in the water column at 35 m occurred during the intense short-rain period (NovembereDecember), consistent with the idea that they were derived from catchment soils mobilized by flood events. However, the distributions of branched GDGTs in a (albeit limited) set of soils from the catchment were slightly different from those in profundal sediments, and a profile of settling particulate matter (SPM) from throughout the water column revealed that concentrations of branched GDGTs (and GDGT-0) were substantially higher below the chemocline (i.e., in permanently anoxic water below 45 m) than in the upper water column. This suggested that in-situ production of branched GDGTs in the lower water column could be an additional source of branched GDGTs in the sediments of Lake Challa. Subsequent studies of a wide variety of lakes have indicated that indeed, in many lakes, in-situ production of branched GDGTs is likely (Sinninghe Damsté et al., 2009; Tierney and Russell, 2009; Bechtel et al., 2010; Blaga et al., 2010; Tierney et al., 2010b; Tyler et al., 2010; Zink et al., 2010; Loomis et al., 2011; Pearson et al., 2011; Sun et al., 2011; Tierney et al., 2012). When the down-core records of the different GDGT ratios in Lake Challa sediments are compared, it is remarkable that the BIT index and %GDGT-0 reveal a strong co-variance (Fig. 4c and d; r2 ¼ 0.87). In SPM collected from the lower water column, both GDGT-0 and branched GDGTs are relatively high in concentration (Sinninghe Damsté et al., 2009), which may suggest that both high BIT index and %GDGT values are caused by an increased contribution of GDGTs from this bottom-water SPM, and thus that in-situ production of branched GDGTs in the anoxic lower water column is the major source for sedimentary branched GDGTs in Lake Challa.

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Fig. 4. The %GDGT-2 (a), %crenarchaeol isomer (b), %GDGT-0 (c), BIT index (d), MBT index (e), and CBT index (f) versus age for the 25 ka record of Lake Challa. The time slices (AeF) discussed in the text are indicated.

The strong co-variation of BIT index and %GDGT could also be caused by variation in the amount of crenarchaeol produced in the lake, since both ratios contain the abundance of crenarchaeol in their definition; high relative amounts of crenarchaeol would result in low BIT index and %GDGT, and vice versa. This is to some extent supported by the record of the %crenarchaeol isomer (Fig. 4b), defined as the relative amount of the crenarchaeol regio-isomer

relative to the sum of crenarchaeol and its isomer (V0 /(V þ V0 ) *100), which shows some co-variation with the BIT index and % GDGT-0 (but note the logarithmic scale of Fig. 4b). It is fairly constant with a declining trend down-core (from ca 2.5%e1%), with elevated values (up to 15%) only in the earliest Holocene and during the LGM, i.e., within those sediment horizons where the BIT index and %GDGT-0 approach 1 and 100, respectively. The %crenarchaeol

J.S. Sinninghe Damsté et al. / Quaternary Science Reviews 50 (2012) 43e54 Table 1 Literature values of the average relative abundance of the crenarchaeol regioisomer. Sample set

Fractional abundance crenarchaeol isomer

Reference

Global soils (n ¼ 118) Kilimanjaro soils (n ¼ 16) Lake Challa catchment (n ¼ 8) Group 1.1a Aquatic Thaumarchaeota (n ¼ 3) Group 1.1b Soil Thaumarchaeota (n ¼ 3)

0.09  0.05

Weijers et al. (2007b)

0.15  0.07

Sinninghe Damsté et al. (2008) Sinninghe Damsté et al. (2009) Pitcher et al. (2011)

0.15  0.04 0.03  0.02

0.21  0.16

Sinninghe Damsté et al. (in press)

isomer values in these two core sections are unusually high, since in comparable datasets the %crenarchaeol isomer ratio for enrichment cultures of aquatic Thaumarchaeota is typically <5% (Table 1). However, for group 1-1b Thaumarchaeota enriched from soils the % crenarchaeol isomer ratio is substantially higher (Sinninghe Damsté et al., in press, Table 1) and indeed in the few Challa soils that have been analysed the %crenarchaeol isomer is also around 15% (Table 1; Sinninghe Damsté et al., 2009). This suggests that the observed down-core changes in %crenarchaeol isomer (Fig. 4b) may be due to relatively small contributions of GDGTs derived from aquatic Thaumarchaeota and relatively high contributions of Thaumarchaeota from soils during certain periods. This would explain the positive correlations between the BIT index and % GDGT-0 and %crenarchaeol isomer ratios. Nevertheless, overall much of the co-variation in the BIT index and the %GDGT-0 and %crenarchaeol isomer ratios appears mainly determined by variation in crenarchaeol production by aquatic Thaumarchaeota in the (upper) water column of Lake Challa, and not by the delivery of branched GDGTs from soil as proposed earlier (Verschuren et al., 2009). If in-situ production of branched GDGTs plays such an important role, an alternative explanation must be sought for why the BIT record (Fig. 4d) might be a good reflection of past rainfall variability, or, more generally, variation in the climatic moisture balance as evident in the seismic stratigraphy of past lakelevel fluctuations (Verschuren et al., 2009).

49

4.1.2. Why does the BIT index reflects the climatic moisture balance? There are two possible reasons for the apparent correlation of the BIT index with moisture balance, which both are related to the nutrient cycling in the lake. Firstly, the negative relationship between wind strength and rainfall in this area (Wolff et al., 2011) may impact BIT index values. In years with low precipitation, more windy dry-season conditions lead to more vigorous and prolonged mixing of the lake’s water column. Below the oxycline (at ca 40 m depth) phosphate and nitrate levels are high, such that more substantial mixing regenerates more nutrients to the surface waters, leading to more extensive blooming of diatom algae (Wolff et al., 2011). Aquatic Thaumarchaeota are nitrifiers (Könneke et al., 2005; Wuchter et al., 2006) and thus depend on primary production as this is ultimately the source of ammonium. At times of strong wind (i.e. limited rainfall), aquatic primary production is enhanced and production rates of crenarchaeol increase, resulting in low BIT index values. Secondly, Verschuren et al. (2009) observed good correspondence between BIT index values and lake level as inferred from seismic-reflection stratigraphy (Moernaut et al., 2010) with high BIT index values at times of high lake level (i.e. time slices F, D and B) and vice versa. When lake level is substantially reduced, turn-over of the water column just above the chemocline at 70 m depth will be much more frequent, enhancing nitrogen recycling in the lake, resulting in a relatively higher production of crenarchaeol, likely resulting in lower BIT index values. A more frequently mixed and thus oxic water column would perhaps also result in less in-situ production of branched GDGTs in the lake since they were predominantly found in the deeper anoxic waters (Sinninghe Damsté et al., 2009). This would also result in lower BIT index values. Reduction of the lake level would be a longer time-scale mechanism for the relationship between rainfall and BIT index, in addition to the shorter-time scale mechanism related to wind strength. Together these mechanisms could thus explain the observed link between rainfall and the BIT index, even if the branched GDGTs are not predominantly derived from erosion of soil organic matter. Although the BIT index and %GDGT-0 are highly correlated in general, this is not always the case for the last 3000 years of the record. In the ternary diagram (Fig. 3) this is evident from about 20 sediment samples in Time slice A (red data points) that contain relatively low amounts (20e40%) of branched GDGTs. When the relative abundance of branched GDGTs to total GDGTs is plotted

Fig. 5. Abundance of the major branched GDGTs (VI, VII, and VIII) relative to all major GDGTs cross plotted against (a) the relative abundance of GDGT-0 (I) relative to all major GDGTs, and (b) sediment age (0e3400 yr BP). Cross plot (a) shows that there is generally a positive correlation (stippled line) in the relative abundance of branched GDGTs and GDGT-0 but not for the first 3400 year (filled data points) when there is a negative correlation (solid line). The thick line in (b) is the 5-point moving average and reveals distinct cycles in the relative abundance of the branched GDGTs with time with minima at 700, 1500, and 2800 yr BP, which represent known periods of lake level low stand in Central Africa.

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against that of GDGT-0 (Fig. 5a), a weak positive correlation is found throughout the record except for those intervals within time slice A with <40% of branched GDGTs. These intervals are noted at around 600e800, 1400e1900 and 2700e2900 yr BP, and minor minima are also evident at w200 and w2300 yr BP (Fig. 5b). These periods also generally have low BIT-index values (Fig. 4d), and at least the three most recent of these (w200, 600e800 and 1400e1900 yr BP) are known from elsewhere to have been relatively dry periods in equatorial East Africa (Verschuren, 1999, 2001; Bessems et al., 2008). Since the lake level did not change substantially over the last 2.5 ka, this suggests that the first mechanism discussed above was probably responsible for the observed changes in the BIT-index during this time interval. 4.2. TEX86 palaeothermometry A proper application of TEX86-based palaeothermometry critically depends on the assumption that GDGTs used for calculation of TEX86 values are all being derived from Thaumarchaeota mainly living in the upper water column. Since various other sources of isoprenoid GDGTs, such as methanogenic archaea in the lower water column or archaea in catchment soils, have now been recognized (Blaga et al., 2009; Powers et al., 2010), we evaluate here the isoprenoid GDGT distributions in Lake Challa to assess if the TEX86 palaeothermometer can be validly applied to this extensive dataset. 4.2.1. Potential non-thaumarchaeotal sources for isoprenoid GDGTs A first validity test is to check for a potential contribution from methanogenic archaea. Blaga et al. (2009) advocated use of the GDGT-0/crenarchaeol ratio, based on the fact that for enrichment cultures of Thaumarchaeota this ratio is always <2, whereas methanogens produce GDGT-0 (and smaller amounts of GDGT-1 and -2) but no crenarchaeol as major GDGTs. We here defined the quantity %GDGT-0 as the contribution of GDGT-0 to the sum of GDGT-0 and crenarchaeol, to make this ratio comparable to the BIT index (see above). The plot of %GDGT-0 versus age (Fig. 4c) often exceeds 67% (implying that GDGT-0/crenarchaeol >2) during the early LGM and both the early and late Holocene, indicating a substantial input of methanogenic GDGTs relative to those of pelagic Thaumarchaeota during the three main periods of high lake level in Lake Challa (Moernaut et al., 2010). Especially during the early Holocene (time slice B), GDGT-0 abundance is remarkably high compared to the other isoprenoid GDGTs (Fig. 2b). This is consistent with our study of GDGT distribution in Lake Challa today (Sinninghe Damsté et al., 2009), which showed by far the highest concentrations of GDGT-0 in SPM from the anoxic lower water column, perhaps originating from methanogenic archaea. Additional evidence for a second source of GDGT-0 in Lake Challa besides Thaumarchaeota was that, at least in the one bottom sediment sample analysed, the stable carbon isotopic composition (d13C) of the tricyclic biphytane originating from crenarchaeol is 5& enriched relative to the acyclic biphytane, which predominantly derives from GDGT-0 (Sinninghe Damsté et al., 2009). Könneke et al. (2012) recently showed that all biphytanes derived from the GDGTs of a thaumarchaeotal culture have identical d13C values. These data suggest a substantial input of methanogenic archaeal GDGTs in Lake Challa and, consequently, TEX86 values obtained from this sediment being unreliable as temperature proxy. Indeed, the plot of TEX86 versus age with coloured symbols for %GDGT-0 values above the cutoff of 67% (Fig. 6a) reveals that exactly these data points deviate from the general rising trend (i.e. the glacial-to-interglacial temperature rise) of TEX86 with decreasing age. Sinninghe Damsté et al. (2009) further noted that GDGT-2 is relatively more abundant than GDGT-1 and GDGT-3 in modern

Fig. 6. TEX86 values versus sediment age for the Lake Challa sediments. Colour coding of the data points indicate other characteristics of the GDGT distribution (a) the % GDGT-0 ratio, (b) the contribution of GDGT-2 relative to the sum of GDGT-1, GDGT-2, GDGT-3 and the crenarchaeol regioisomer, and (c) the BIT ratio.

surface and sub-surface (<30 cm) profundal sediments in Lake Challa, as is also the case in time slices A, B and D (Fig. 2a,b and d). The quantity %GDGT-2, which is the contribution of GDGT-2 relative to the sum of minor GDGTs (GDGT-1, -2, -3, and the crenarchaeol isomer) in modern-day Lake Challa sediments (ca 55%) is substantially higher than in marine surface sediments, where it varies from 20 to 45% depending on the temperature of the surface ocean (Kim et al., 2008). However, this phenomenon was not observed in settling particles at 35 m depth or in SPM from the anoxic lower water column (Sinninghe Damsté et al., 2009). This strongly suggests that GDGT-2 has a different source than other isoprenoid GDGTs that derive from Thaumarchaeota residing in the

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Fig. 7. TEX86 records for Lake Malawi (Powers et al., 2005), Lake Tankanyika (Tierney et al., 2008) (a) and Lake Challa (b). The axes on the right provide LST estimates using the Powers et al. (2010) (primary axis) and Tierney et al. (2010a) (secondary axis) lake calibrations, respectively. Only TEX86 data points of the Challa sedimentary record were used that remain after applying various filters on the data as discussed in the text. The thick lines give the 5-point moving average.

upper water column (but excluding GDGT-0; see discussion above). In the sediment record of Lake Challa studied here, %GDGT-2 for most of the Holocene, Younger Dryas and early Lateglacial sediments is also >50%, whereas for older sediments its values are <45% (Fig. 4a). The plot of TEX86 versus age with coloured symbols for high %GDGT-2 values (Fig. 6b) now reveals that generally data points with high TEX86 values are also characterized by high % GDGT-2 values. In part this trend is caused by the fact that %GDGT-2 is responsive to temperature (Kim et al., 2010), and thus that elevated %GDGT-2, causing higher TEX86, simply reflects higher temperatures. However, Sinninghe Damsté et al. (2009) previously argued that strongly elevated relative amounts of GDGT-2 cause ‘too high’ values for TEX86; if transformed to lake temperatures using the calibration of Powers et al. (2010), unrealistically high temperatures are obtained. Thus, using an upper limit of 45% GDGT2 based on Kim et al. (2008), TEX86 values for almost all Holocene sediments in Lake Challa, as well as some samples from the period 12e17 ka BP, are likely not suitable for TEX86 palaeothermometry. A third way of judging if GDGT distributions are suitable for TEX86 palaeothermometry involves close examination of the BIT index. Blaga et al. (2009) advocated its application in lakes because branched GDGTs at that time were thought to be a tracer for soil-

derived organic matter in the lake. Since soils also contain isoprenoid GDGTs, substantial input of soil organic matter into a lake can alter the isoprenoid GDGT distribution produced in-situ by Thaumarchaeota. A cut-off value of 0.4 for the BIT index was recommended (Blaga et al., 2009). With the new insight that branched GDGTs can also derive from in-situ production (Sinninghe Damsté et al., 2009; Tierney and Russell, 2009; Bechtel et al., 2010; Blaga et al., 2010; Tierney et al., 2010b; Tyler et al., 2010; Zink et al., 2010; Loomis et al., 2011; Pearson et al., 2011; Sun et al., 2011; Tierney et al., 2012) and that absolute values for the BIT index vary between labs (Schouten et al., 2009), absolute BIT index values can no longer be used to quantify the input of soil organic matter into lakes. However, plotting TEX86 values versus age with coloured symbols for elevated BIT index values (Fig. 6c) reveals that these data points are basically the same as those with a high %GDGT0 value (Fig. 6a). This is to be expected, since the BIT and %GDGT0 are highly correlated (Fig. 4c and d, and their discussion above). 4.2.2. Filtering the Challa TEX86 record When Lake Challa sediment samples with %GDGT-0 values >67 and/or %GDGT-2 values >45 are excluded, ca 60 horizons remain that have GDGT distributions and TEX86 values consistent with

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their dominant source being the pelagic Thaumarchaeota. These data points are all from the time interval between 13 and 25 ka BP, with only a few younger than 16.5 ka BP (Fig. 7b). Using the lakebased TEX86 calibration of Powers et al. (2010) to calculate mean LST (Equation (5)) yields temperatures between 12 and 24
C (Fig. 7b). Starting at 25 ka BP, LST is more or less constant at 13
C throughout the LGM, followed by a sharp rise to 15e16
C dated to ca19.2 ka BP. This rise continues throughout the Lateglacial period until a LST of 21e22
C is reached just before the Younger Dryas (Fig. 7b). This temperature approaches the 22
C calculated from the flux-weighted annual average TEX86 value of 0.65 for descending particles collected at 35 m depth in Lake Challa today (Sinninghe Damsté et al., 2009). Tierney et al. (2010b) recently proposed an alternative TEX86 calibration for African lakes (Equation (6)). Application of this calibration results in a smaller amplitude of temperature variations, between 15
C for the LGM and 21e22
C just before the YD (Fig. 7b). The amplitude of post-glacial warming reconstructed with TEX86 for Lake Challa (5.5e10
C depending on the calibration; Fig. 7b) is relatively large compared with TEX86 records from the large African rift lakes Malawi and Tanganyika, which reveal a warming of 3e5
C (Fig. 7a) from the LGM to the start of the Holocene (Powers et al., 2005; Tierney et al., 2008; Woltering et al., 2011). However, the inferred timing of the onset of post-glacial warming in tropical Africa is consistent among all three lakes (Fig. 7). It is especially the low LST values for Lake Challa (13e15.5
C) during the LGM that seem incompatible with other climate data from Africa for this time period. This may indicate that specific local and regional factors caused anomalously low LST in Lake Challa. We tentatively attribute this result to glacial Lake Challa water-column temperatures being markedly lower than ambient mean glacial air temperatures. The modern water budget of Lake Challa is dominated by sub-surface inflow from precipitation higher up on Mt. Kilimanjaro (Payne, 1970), where annual rainfall peaks at w2000e2500 m asl in the montane forest zone (Hemp, 2006). If LGM and early Lateglacial rainfall was significantly reduced compared to today (e.g., 25%: Hostetler and Clark, 2000), the steeper lapse rate of the drier atmosphere (Farrera et al., 1999) would have caused the lake’s water budget to be dominated by cold subsurface inflow. We surmise that this may have resulted in enhanced temperature contrast between water and ambient air temperature. An alternative hypothesis that the large local LGM DT could be related to the cooling influence of an expanded Mt. Kilimanjaro ice cap on air temperature in surrounding lowlands has less merit. At LGM, Mt. Kilimanjaro glaciers expanded to w150 km2, with their Equilibrium Line Altitude (ELAg) at 4300e4240 m (830  160 m lower than today) and glaciers on the Mawenzi side (facing Lake Challa) terminating at 3250 m (Porter, 2001). In the Rwenzori, LGM ice cover was w260 km2, ELAg was at 3600 m and glaciers terminated at 2070 m. The steeper lapse rate caused the LGM DT at 1500e2000 m to be 5
C greater than at 500 m (Kageyama et al., 2005). Thus, lakes nearby glacier termini in the Rwenzori would likely have recorded a greater LGM DT than lowland lakes. However, given that Mt. Kilimanjaro glaciers terminated 2400 m above Lake Challa’s elevation, it is doubtful that cooling by an expanded ice cap can be invoked to explain the large LGM DT inferred from the TEX86 reconstruction.

derive from terrestrial soils, this calibration can also be used to reconstruct MAAT. However, recent studies have shown that MBT/ CBT-inferred modern-day temperatures in lacustrine settings are far too low, up to 30
C in some extreme cases (Blaga et al., 2010; Tierney et al., 2010b; Zink et al., 2010; Loomis et al., 2011; Sun et al., 2011). Indeed, using the soil calibration (Weijers et al., 2007b) to calculate past MAAT from the MBT and CBT values measured in the Lake Challa core sequence, produces temperatures between 2 and þ12
C (data not shown), unrealistically low for an equatorial lake even during peak glacial times. These values appear to confirm that the branched GDGTs in Lake Challa sediments are not predominantly derived from terrestrial soils but are mainly produced within the lake. Tierney et al. (2010b) produced a potentially more relevant MBT/CBT calibration from the recent bottom sediments of 40 African lakes. Application of this calibration (Equation (8)) to the Challa sediment record produces MAAT values of 19e22
C for the Holocene and 17e19
C for the (early) LGM, separated by an inferred cold period 20e13 ka BP when temperatures are inferred to have dropped to as low as 12
C around 15 ka BP (Fig. 8a). Application of an MBT/CBT calibration based on lake-sediment samples with global distribution (Equation (9); Pearson et al., 2011) returns a similar temperature history for the Lake Challa region, except that Holocene MAAT estimates are w2
C higher, and LGM and Lateglacial estimates are w1
C higher (Fig. 8a). Both lakebased MBT/CBT calibrations infer a difference in MAAT between the LGM and the Holocene of 4e5
C, i.e. in good agreement with other African temperature records (Powers et al., 2005; Weijers et al., 2007a; Tierney et al., 2008). However, the distinct cooling phase between 20 and 13 ka BP is not seen in any other regional record. Again one could argue that perhaps a large input of melt-water from the retreating glacial-era ice cap on Mt. Kilimanjaro caused anomalous cooling of Lake Challa (cf. TEX86). However, this meltwater would have had to go underground during its descent from the mountain, since today no trace exists of a ravine or formerly active river course providing melt-water input to Lake Challa. We do note, however, that a brief episode of warming interrupting this inferred Lateglacial cold period at 16e17 ka BP coincides with seismic-reflection evidence for the most pronounced low stand of Lake Challa (Moernaut et al., 2010) in the last 25,000 years, interpreted by these authors as a possible local signature of the Heinrich I event (Hemming, 2004).

4.3. MBT/CBT palaeothermometry The MBT/CBT palaeothermometer was developed for branched GDGTs eroded from soils and transported to coastal marine sediments by rivers (Weijers et al., 2007a,b) and calibrated using a large set of soil samples with wide geographical distribution (Weijers et al., 2006a,b). If branched GDGTs in lake sediments likewise

Fig. 8. Reconstructed temperature versus sediment age using the MBT and CBT index data of the Challa sedimentary record. For determination of temperature the African lake (black line; Tierney et al., 2010b) and global lake (blue line; Pearson et al., 2011) calibration were applied. The thick line represents the 3-points moving average.

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5. Conclusion Our results show that the distribution of isoprenoid and branched GDGTs in lake sediments clearly has potential to reconstruct palaeoenvironmental and palaeoclimatic signals once potential biases are properly constrained. Sources of isoprenoid GDGTs other than Thaumarchaeota, such as methanogenic archaea, can affect TEX86 values and render TEX86 palaeothermometry impossible. However, specific methods based on the GDGT distributions of these other archaea can be applied to filter the TEX86 record and generate more reliable records of LST. Application of this method revealed a substantial warming of 6e10
C of Lake Challa during the deglaciation depending on the calibration used. Variation in down-core values of the BIT index are, in contrast to earlier ideas, mainly determined by the varying production rate of crenarchaeol relative to in-situ produced branched GDGTs. The apparent relationship of BIT with climatic moisture balance is probably due to either the direct influence of lake level and wind strength on nutrient recycling, or to influx of soil nutrients promoting aquatic productivity and nitrification. Finally, branched GDGTs record realistic temperatures for the LGM and Holocene but detailed knowledge on the origin of branched GDGTs and the impact of physical parameters such as temperature is required before these data can be interpreted with full confidence. Acknowledgements This study was carried out with permission of the Permanent Secretary of the Ministry of Education, Science and Technology of Kenya under research permit 13/001/11C to DV. We thank Dr E.C. Hopmans for help with LC/MS analyses. This work was partly performed under the umbrella of the ESF Euroclimate project CHALLACEA, financially supported by grants from the Dutch Organization for Scientific Research (NWO) and FWO-Vlaanderen (Belgium) to JSSD and DV, respectively. The research leading to these results has also received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007e2013)/ERC grant agreement n
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