Quaternary Science Reviews 87 (2014) 24e33
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Quaternary Science Reviews
journal homepage: www.elsevier.com/locate/quascirev
Abundant C4 plants on the Tibetan Plateau during the Lateglacial and
early Holocene
Elizabeth K. Thomas a, *, Yongsong Huang a, Carrie Morrill b, Jiangtao Zhao c,
Pamela Wegener a, Steven C. Clemens a, Steven M. Colman d, Li Gao a, e
a
Department of Geological Sciences, Brown University, Box 1846, Providence, RI 02912, USA
Cooperative Institute for Research in Environmental Sciences, University of Colorado and NOAA National Climatic Data Center, Boulder, CO 80305, USA
State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, Chinese Academy of Sciences, Xi’an 710075, China
d
Large Lake Observatory, University of Minnesota, Duluth, MN 55812, USA
e
GeoIsoChem Corporation, 738 Arrow Grand Circle, Covina, CA 91722, USA
b
c
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 14 October 2013
Received in revised form
12 December 2013
Accepted 17 December 2013
Available online 24 January 2014
Plants using the C4 (Hatch-Slack) photosynthetic pathway are key for global food production and account
for ca 25% of terrestrial primary productivity, mostly in relatively warm, dry regions. The discovery of
modern naturally-occurring C4 plant species at elevations up to 4500 m in Tibet and 3000 m in Africa and
South America, however, suggests that C4 plants are present in a wider range of environments than
previously thought. Environmental conditions on the Tibetan Plateau, including high irradiance, rainfall
focused in summer, and saline soils, can favor C4 plants by offsetting the deleterious effects of low
growing season temperature. We present evidence based on leaf wax carbon isotope ratios from Lake
Qinghai that C4 plants accounted for 50% of terrestrial primary productivity on the northeastern Tibetan
Plateau throughout the Lateglacial and early Holocene. Despite cold conditions, C4 plants flourished due
to a combination of factors, including maximum summer insolation, pCO2 ca 250 ppmv, and sufficient
summer precipitation. The modern C3 plant-dominated ecosystem around Lake Qinghai was established
ca 6 thousand years ago as pCO2 increased and summer temperature and precipitation decreased. C4
plants were also intermittently abundant during the Last Glacial period; we propose that C4 plants
contributed a significant portion of local primary productivity by colonizing the exposed, saline Qinghai
Lake bed during low stands. Our results contrast with state-of-the-art ecosystem models that simulate
<0.5% C4 plant abundance on the Tibetan Plateau in modern and past environments. The past abundance
of C4 plants on the Tibetan Plateau suggests a wider temperature range for C4 plants than can be inferred
from modern distributions and model simulations, and provides paleoecological evidence to support
recent findings that C4 plant evolution and distribution was determined by a combination of climatic and
environmental factors (temperature, irradiance, precipitation amount and seasonality, and soil salinity).
Moreover, this finding highlights the exceptional sensitivity of high-elevation ecosystems to environmental change, and provides critical benchmarks for ecosystem model validation.
Ó 2013 Elsevier Ltd. All rights reserved.
Keywords:
Leaf wax
Carbon isotope
C4 photosynthesis
Paleoecology
Tibetan Plateau
Monsoon
1. Introduction
Under present atmospheric CO2 concentrations, C4 plants are
minor or absent in cool, high-elevation environments (Ehleringer
et al., 1997; Collatz et al., 1998; Sage et al., 1999; Edwards and
Smith, 2010). The modern distribution of C4 plants is likely a
result of preferential adoption of C4 photosynthesis by clades
adapted to warm, mesophytic conditions (>22 C mean growing
* Corresponding author. Tel.: þ1 716 417 3062.
E-mail address: [email protected] (E.K. Thomas).
0277-3791/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.quascirev.2013.12.014
season temperature, ca 1200 mm yr1 rainfall), where the C4
photosynthetic pathway imparts a competitive advantage (Collatz
et al., 1998; Edwards and Smith, 2010). Ecosystem models incorporate a 22 C minimum mean monthly temperature requirement
for C4 plants in addition to a 25 mm month1 minimum precipitation threshold for all plants (Collatz et al., 1998; Still et al., 2003).
Therefore, these models reconstruct few C4 plants at latitudes >50
or elevations >2500 m asl (e.g., Fig. 1), which may result in underestimates of global primary production (Still et al., 2003).
The existence of >50 C4 plant species on the Tibetan Plateau and
other high-elevation regions challenges this 22 C threshold criterion (Fig. S1; Tieszen et al., 1979; Cavagnaro, 1988; Wang et al.,
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
25
plant abundance reconstruction with the CCSM3 transient simulation of C4 plant abundance.
1.1. Setting
Fig. 1. Location map. Lake Qinghai (black) and catchment (dark gray), Tibetan Plateau
(light gray), modern boundary of 5% C4 plants (thick black line; Still et al., 2003), and
sites mentioned in text (white dots; H, Huanxian; W, Weinan (Liu et al., 2005); X,
Xunyi (Zhang et al., 2003); M, Mangshan (Peterse et al., 2011)). C4 plants abundance is
variable and heterogenous, ranging from 0 to 80% in Southeast Asia, the Philippines,
and Indonesia (Still et al., 2003). Inset: C4 grass abundance at 9 ka simulated with the
CCSM3 transient simulation (Z. Liu et al., 2009), showing no C4 grasses on the Tibetan
Plateau, but consistent minor C4 grass abundance in Southeast Asia, the Philippines,
and Indonesia (white; see Fig. S5 for more time slices).
2004) and indicates that C4 plants can successfully compete with C3
plants at high-elevations despite cold conditions, given other
environmental conditions that favor C4 plants (Pyankov et al.,
2000). Such conditions include 20% higher irradiance than at sea
level, >50% of rainfall falling in summer, and high salinity soils (up
to 10 ppt; Baogen et al., 2013). Furthermore, the evolution of C4
photosynthesis in cold-, arid-, salt-adapted clades, such as Chenopodiaceae sensu stricto (s.s.), eudicotyledonous plants that are
abundant in Asian deserts, may eliminate strict temperature limitations for some C4 plants (Pyankov et al., 2000; Kadereit et al.,
2012).
The Tibetan Plateau and other high-elevation regions experience amplified responses to global climatic change due to cloudand snow-albedo feedbacks (X. Liu et al., 2009; Diffenbaugh et al.,
2012). High-elevation plant ecosystems must adapt to amplified
climatic change under already harsh (cold, arid) conditions, and are
therefore bellwethers of climatic and environmental change. Reconstructions of plant ecosystem variability during climate regimes
different than today elucidate mechanisms that cause plant
ecosystem change, and provide information to improve ecosystem
model accuracy in sensitive high-elevation regions.
We present a sub-millennial-resolution 32-ka-long reconstruction of C4 plant abundance on the northeastern Tibetan Plateau
based on d13C of leaf wax C28 n-acids (d13Cwax) from Lake Qinghai
(37 N, 100 E, 3194 m above sea level; Fig. 1). We augment our
findings with a 16-ka-long pollen record from Lake Qinghai (Ji et al.,
2005); a detailed interpretation of the 32-ka-long pollen record is
in preparation (S. Xue, personal communication). Our work builds
on research by An et al. (2012), who developed an age model and
initial climate reconstructions from the Lake Qinghai drill cores. We
compare our C4 plant abundance reconstruction with existing
climate, environmental, and ecological records. We use output from
a 21-ka-long transient simulation of the Community Climate System Model 3 (CCSM3) to evaluate past seasonal temperature and
precipitation changes around Lake Qinghai. We also compare our C4
Lake Qinghai is well suited for evaluating average landscape
properties because æolian and fluvial processes deliver leaf waxes
to the closed-basin lake from a large catchment (30,000 km2) at
high-elevations (3194 to >4000 m above sea level; An et al., 2012).
Today, Lake Qinghai’s catchment contains temperate and alpine
steppe vegetation, dominated by C3 Poaceae and Artemisia (Chen
and Peng, 1993; Herzschuh et al., 2009). Mean annual precipitation is 370 mm, with 60% falling in June through August; mean
annual evaporation is >1000 mm (“China Meteorological Data
Sharing Service System,” 2012). The average temperature for July,
the warmest month, is 16 C.
In the Lake Qinghai catchment, May is the first month with
average surface temperatures above 0 C, so is the month when C3
plants begin to grow, if there is enough precipitation and/or snow
melt. In contrast, C4 plants thrive during the summer, when temperature is highest, but only when there is sufficient moisture. We
use these basic guidelines to interpret our record of C4 plant
abundance.
1.2. Determining past C4 plant abundance
Different enzyme-mediated reactions in the C3 and C4 photosynthetic pathways impart distinct carbon isotope compositions on
plant biomass: C4 plants are ca 15& enriched in 13C relative to C3
plants (O’Leary, 1981). These distinct d13C compositions are also
reflected in leaf waxes (Chikaraishi and Naraoka, 2007; Rao et al.,
2008). Leaf waxes are n-alkyl lipids that form a protective layer
on leaves; plants in arid regions produce particularly high abundances of leaf waxes (Shepherd and Griffiths, 2006). Leaf waxes are
abraded from the leaf surface and carried to a lake basin by wind
and/or water and are preserved well in Quaternary lake sediments
(Castañeda and Schouten, 2011). We use leaf wax isotopic endmember values for C3 and C4 plants, discussed below, to calculate
C4 plant abundance.
2. Methods
2.1. Lipid biomarker extraction and purification
131 samples were obtained from ICDP drill cores LQDP05 1A and
LQDP05 1F for organics analysis. The stratigraphy, age model, and
initial climate reconstructions for these drill cores are described in
previous work (An et al., 2012). Free lipids were extracted from
freeze-dried samples with an Accelerated Solvent Extractor 200
(Dionex) using dichloromethane (DCM):methanol 9:1 (v:v). Nalkanoic acids were prepared by first separating the TLEs on solid
phase Aminopropyl silica gel flash columns using three column
volumes of DCM:Isopropanol 2:1 (v:v) and 4% acetic acid in diethyl
ether. The acid fraction was methylated in anhydrous 5% HCl in
methanol at 60 C overnight. Hydroxyl-carboxylic acids were
removed from the methylated acid fractions using silica gel flash
columns with DCM as the eluant, after eluting apolar compounds
with hexane.
2.2. Carbon isotope analysis
The carbon isotope ratio of fatty acid methyl esters (FAMEs) was
determined on an HP 6890 gas chromatograph interfaced to a
Thermo Finnigan Delta Vplus isotope ratio mass spectrometer
through a combustion reactor at Brown University. Isotope values
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E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
are expressed in per mille (&) relative to Vienna Pee Dee Belemnite
(VPDB). The FAME d13C values were corrected for the isotopic
contribution of the carbon in the methyl group added during
methylation. The analytical error, calculated using the results of
duplicate analyses of each extract, is 0.4& (1s) and an external
FAME standard, injected once after every sixth sample injection,
had an analytical error of 0.7& (1s).
2.3. Transient simulation
The transient simulation of the past 21,000 years was carried out
using the low-resolution version (T313) of the Community
Climate System Model, version 3 (CCSM3; Z. Liu et al., 2009; He,
2011; Liu et al., 2012). CCSM3 is a global, ocean-atmosphere-sea
ice-land surface climate model coupled without flux corrections.
The atmospheric component is the Community Atmosphere Model
version 3 at a horizontal resolution of T31 (approximately 3.75 in
latitude and longitude) and 26 hybrid vertical levels. The land
model, which predicts plant functional types using a dynamic
vegetation scheme, uses the same grid as the atmospheric
component. The ocean model is an implementation of the Parallel
Ocean Program model with longitudinal resolution of 3.6 and
variable latitudinal resolution, with finer resolution in the North
Atlantic and tropics (w0.9 ). The vertical resolution is 25 levels
extending to a depth of 5.5 km. The dynamicethermodynamic sea
ice model uses the same horizontal grid and land mask as the ocean
component. The T313 present-day control simulation reproduces
the major features of global climate, with improved ocean circulation compared to earlier versions of this model (Yeager et al.,
2006). Results from the higher-resolution (T421) version of
CCSM3 for Last Glacial Maximum and middle Holocene conditions
capture important paleoclimate patterns documented by proxy
records (Otto-Bliesner et al., 2006).
Detailed information about the forcings used in the transient
experiment can be found in He (2011), Liu et al. (2012), and Z. Liu
et al. (2009). Briefly, orbital forcing varied transiently (Berger,
1978), and greenhouse gas (CO2, CH4, and N2O) concentrations
were based on ice core measurements (Joos and Spahni, 2008).
Continental ice sheets were based on the ICE-5G reconstruction
(Peltier, 2004) and altered approximately once per thousand years.
Meltwater forcing (MWF) prior to 14.5 ka was the DGL-A scheme (Z.
Liu et al., 2009), which includes an abrupt termination at the
Bolling-Allerod. Following this, major periods of MWF were prescribed from 14.4 to 13.9 ka to the North Atlantic and Southern
Ocean and from 12.9 to 11.7 ka and from 9.0 to 8.2 ka to the North
Atlantic (He, 2011; Liu et al., 2012).
To generate time series of climate variables from the transient
simulation for the Lake Qinghai area, we averaged the four closest
grid cells to the lake (Fig. 2). This choice was made to average out
random fluctuations from individual grid cells while accounting for
the relatively low resolution of the model and the large topographic
gradients in this region. The transient evolution of temperature and
precipitation for these four grid cells is representative of
monsoonal Asia as a whole (Figs. 2, S2 and S3).
Fig. 2. Surface temperature, precipitation, and moisture balance (precipitation minus
evaporation) time series from the CCSM3 transient simulation (Z. Liu et al., 2009). Each
time series was produced from the average of four grid cells surrounding Lake Qinghai
(Figs. S2 and S3). Average winter (DecembereFebruary) variables plotted in black; May,
June, July, and August variables plotted individually. Simulated modern temperatures
are cooler than modern observations (“China Meteorological Data Sharing Service
System,” 2012), likely because modern observations are point measurements and
the model temperatures are averaged over a large area. Nonetheless, the magnitude of
glacialeinterglacial-scale modeled temperature change is similar to reconstructed
temperature change on the CLP.
(years 1986e2005 AD). We used all models in the CMIP5 archive as
of May 2013 that provided the information necessary for our
analysis (Table S1). For models providing ensembles for the RCPs,
we analyzed just one ensemble member given the expectation that
differences among the models are typically larger than differences
between ensemble members. The grid resolutions vary among the
models and to ensure that we consistently averaged the same
spatial area we first bilinearly interpolated results from all models
to the CCSM4 grid. Then, we calculated the area average for a
3 3 box centered on the location of Lake Qinghai (37 N, 100 E).
3. C28 n-acid carbon isotopes as a proxy for C4 plant
abundance
2.4. CMIP5 model results
3.1. Leaf wax sources
To provide an estimate of conditions that the Tibetan Plateau
plant ecosystem will be experiencing in ca 2050 AD, we extracted
temperature and pCO2 data for the Tibetan Plateau from Coupled
Model Intercomparison Project Phase 5 (CMIP5) model projections.
Temperature and precipitation anomalies for the Lake Qinghai area
at ca 2050 AD were calculated from CMIP5 model projections, using
the Representative Concentration Pathways (RCP) 2.6 and 8.5
(years 2040e2059 AD) relative to historical climate simulations
The most abundant n-acid chain lengths in Lake Qinghai sediments are C26 and C28. Terrestrial plants in the modern Lake
Qinghai catchment produce mainly mid- to long-chain n-acids,
with a peak at C24; C26 and C28 n-acids compose ca 10% each of total
terrestrial plant leaf wax production (Wang and Liu, 2012). In
contrast, aquatic plants produce mainly C16 n-acids. C26 is <10%,
and C28 is <5% of total aquatic plant leaf wax production (Wang and
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
Liu, 2012). Aquatic pollen is a minor component (<1% average) of
the total pollen flux throughout the entire 32-ka record, except
from 20.5 to 15.5 ka, when aquatic pollen averages 5%, and briefly
peaks at 65% at ca 18 ka (Fig. 3; Ji et al., 2005; S. Xue has generated
aquatic pollen data for the past 32 ka in Lake Qinghai and reconstructs pollen abundance up to 65% at 20.5, 18, and 15.5 ka,
personal communication). Terrestrial plants are therefore the
dominant source of long-chain n-acids, with the possible exception
27
of brief intervals between 20.5 and 15.5 ka. We report d13C of the
C28 n-acid because aquatic plants produce fewer C28 n-acids, and
are less likely to contaminate the terrestrial signal.
3.2. Carbon isotope end members
In order to convert d13Cwax to C4 plant abundance, we must
determine reasonable C3 and C4 plant C28 n-acid d13C values for the
Fig. 3. Lake Qinghai d13Cwax compared to local precipitation and pollen reconstructions. A. Qinghai d13Cwax. Error bars on data points are 1s analytical precision. Horizontal black
and gray bars are 14C age constraints, shown with 1s calibrated range; gray arrows and numbers indicate reservoir correction applied to ages of the same shade, Holocene ages had a
135-year reservoir correction; black stars indicate depths of 14C ages that are >20 ka older than their depositional age based on this age model (An et al., 2012). B. Inferred C4 plant
abundance and uncertainty calculated using likely range of C3 and C4 plant end member 13Cwax values (solid black line and gray range). Thin black line shows 0% C4. C. Lake Qinghai
ostracode d18O (Liu et al., 2007), age model adjusted to match age model from ref. (An et al., 2012). Negative values in the early Holocene indicate more summer precipitation (2s
analytical error is 0.2&). D. Percent carbonate and flux of large grains in Lake Qinghai sediments (An et al., 2012). Higher %CaCO3 in the Holocene likely indicates more precipitation, the increase at 11.5 ka is likely due to a sedimentological transition as well as a precipitation increase. Larger grain size flux corresponds to stronger westerly winds, and
likely greater winter precipitation. E. Percent Poaceae, Chenopodiaceae s.s., tree, and aquatic pollen, and pollen concentration in Lake Qinghai sediments (Ji et al., 2005). Age model
from Ji et al. (2005) adjusted to match age model for our samples by correlating percent total organic carbon from the two records. Gray bars highlight Younger Dryas and Heinrich
Events 1e3, defined by 18O-enriched intervals in the Chinese speleothem records (Wang et al., 2008).
28
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
Tibetan Plateau. We are not aware of any published modern C28 nacid d13C values for this region. We use C28 n-acid d13C values for C3
and C4 plants at lower elevations, adjusted for known effects of
elevation and aridity, to determine end member values for the Tibetan Plateau.
3.2.1. C3 plant d13Cwax end member
The d13C of C28 fatty acid in C3 trees and herbs from Thailand and
Japan, where mean annual precipitation is ca 1500 mm,
is 36.9 1.7& (Chikaraishi and Naraoka, 2007). When C3 plants
are drought-stressed, as is the case for plants on the northeastern
Tibetan Plateau, their biomass becomes enriched in 13C by up to 3&
relative to non drought-stressed C3 plants (Passey et al., 2002). A
compilation of carbon isotope fractionation during CO2 uptake and
fixation (Dleaf) by trees throughout the world shows that trees in
dry regions have lower Dleaf, and therefore higher d13C, than trees in
wet regions, even within a single genus (Diefendorf et al., 2010). C3
plants at higher elevations also have lower Dleaf, perhaps due to
decreased atmospheric pressure (Li et al., 2007; Diefendorf et al.,
2010; Zhou et al., 2011). Assuming that this relationship applies
to grasses and herbs as well as trees, we apply an empirically
derived equation for leaf d13Cwax enrichment: Dleaf ¼ 4.20(0.26)
*log10(MAP) 0.06(0.01)*Oaltitude þ 9.31(0.90), MAP ¼ mean
annual precipitation in mm, (Diefendorf et al., 2010) using an
average catchment MAP of 370 mm and an elevation of 3500 m. The
combination of aridity and high-elevation at Lake Qinghai would
cause up to 5.3 2.2& enrichment of C3 plant d13Cwax compared to
plants in Japan and Thailand (Chikaraishi and Naraoka, 2007;
Diefendorf et al., 2010). The modern landscape around Lake Qinghai is dominated by C3 plants, and the minimum late Holocene
d13Cwax in Lake Qinghai sediments is 32.9&. This is 4& enriched
in 13C relative to d13Cwax of C3 trees and herbs in Japan and Thailand,
close to the predicted 5.3& enrichment. We therefore
use 33 2& for the C3 plant d13Cwax end member at Lake Qinghai.
The glacial period was drier than the Holocene at Lake Qinghai
(Colman et al., 2007; An et al., 2012), likely causing C3 plant d13C to
be more enriched. Although we do not have quantitative estimates
of precipitation amount, a site with 100 mm growing season precipitation would contain C3 plants 2& enriched relative to modern
C3 plants at Lake Qinghai using the equation above (Diefendorf
et al., 2010). Thus, the glacial C3 plant d13Cwax end member value
may have been closer to 31&, which would decrease our calculated C4 plant abundance during the glacial period by 5e10%
(Fig. 3B). Note that the 31& C3 plant d13Cwax end member results
in negative C4 plant abundance during the late Holocene, and is
therefore likely only applicable to the glacial period.
3.2.2. C4 plant d13Cwax end member
The d13C of C28 fatty acid in C4 plants from Thailand and Japan,
where mean annual precipitation is ca 1500 mm, is 21.4 2.1&
(Chikaraishi and Naraoka, 2007). Unlike C3 plants, drought-stressed
C4 plants do not exhibit changes in biomass d13C (Passey et al.,
2002). Drier conditions on the Tibetan Plateau, or changes in precipitation amount between the glacial and Holocene periods likely
do not affect the C4 plant d13Cwax end member. There is evidence
that C4 Chenopodiaceae s.s., a dominant form of C4 plants in central
Asian deserts, have lower Dleaf at high-elevations (0.1& per 100 m;
Pyankov et al., 2000; Van de Water et al., 2002). At 3500 m on the
northeastern Tibetan Plateau, the C4 plant d13Cwax end member
value would be 18&, ca 3& enriched in 13C relative to C4 plant
d13Cwax at low elevations (Chikaraishi and Naraoka, 2007).
3.2.3. Aquatic plant d13Cwax end member at Lake Qinghai
Aquatic plants are intermittently abundant in the Lake Qinghai
record (Fig. 3; Ji et al., 2005). Aquatic pollen in the Lake Qinghai
record is mainly Myriophyllum sp. with minor amounts of Potamogeton sp. and Sparganium sp. Carbon isotopes of bulk Potamogeton sp. material from Lake Qinghai are 17.8 to 15.9& (W. Liu
et al., 2013). Cladophora sp., aquatic phytoplankton that do not
produce pollen and produce only a small relative proportion of long
chain n-acids, have bulk carbon isotope values of 33.6 to 28.6&
(Wang and Liu, 2012; W. Liu et al., 2013). C28 n-acid carbon isotopes
tend to be depleted relative to bulk values, and therefore the bulk
values cited here are maxima for aquatic d13Cwax end members. The
studies of plants at Lake Qinghai do not provide information
regarding the concentration of n-acids produced by aquatic and
terrestrial plants, although other research demonstrates that
terrestrial plants produce more n-acids than aquatic plants (Gao
et al., 2011). Aquatic plants are therefore unlikely to have contributed significant amounts of n-acids to the Lake Qinghai sediments
throughout most of the record. One exception to this is the interval
at 18 ka, when aquatic pollen is >65% (S. Xue, personal communication). Depleted d13Cwax values, ca 34&, also occur in this interval, and may be a result of increased aquatic plant productivity,
particularly Cladophora sp., which has depleted bulk d13C values.
3.3. C4 plant abundance, error estimates, and alternate
interpretations
Lake Qinghai d13Cwax ranges from 32.9 to 21.9& (Fig. 3).
d13Cwax was most 13C-depleted from 32 to 21 ka and 6 to 0 ka and
most 13C-enriched during the Lateglacial and early Holocene (13.7e
8.3 ka; Fig. 3). This 10& range is most likely a result of changing C3
and C4 plant biomass in the Lake Qinghai catchment. We therefore
use the isotopic end members, 33 2& for C3 plants and a range
from 21 to 18& for C4 plants, and the Lake Qinghai d13Cwax record to calculate C4 plant abundance from 32 ka to the Late Holocene (Fig. 3B; black line end members: 33& for C3 and 18& for
C4 plants). C3 plants were dominant (>80%) during the glacial
period, with two intervals of abrupt C4 plant expansion. During the
Lateglacial and early Holocene, C4 plants were abundant (ca 50%) in
the Lake Qinghai catchment. The modern C3-dominated ecosystem
developed ca 6 ka. Due to uncertainty in our end member estimates, we present a range of possible C4 plant abundance (Fig. 3B).
We stress that aridity-driven changes in C3 plant 13CO2
discrimination would cause d13Cwax variations no greater than
ca 3&. If aridity were the main cause of changes in Lake Qinghai
d13Cwax, the dry late Holocene would be more enriched in 13C than
the wet early Holocene (Passey et al., 2002; Wang et al., 2003;
Diefendorf et al., 2010; An et al., 2012; Dietze et al., 2013; Hudson
and Quade, 2013). This is opposite the trend that we observe
(Fig. 3). Furthermore, CAM plants, such as Crassulaceae and Isoetes,
are rare in this part of the Tibetan Plateau, in both modern surveys
and in the pollen record, and so would likely not influence d13Cwax
(Chen and Peng, 1993; Ji et al., 2005; Herzschuh et al., 2010). Thus,
we interpret the Lake Qinghai d13Cwax record as indicating changes
in terrestrial plant ecology, specifically changes in C3 and C4 plant
biomass.
4. Discussion
We propose that two distinct sets of environmental conditions
caused C4 plants to flourish in the Lake Qinghai catchment: 1. From
21 to 15 ka: C3 plants dominated, but arid conditions caused Lake
Qinghai level to drop, exposing the lake bed, which was colonized
by early-succession, cold- and salt-tolerant C4 Chenopodiaceae s.s.
and, 2. During the Lateglacial and early Holocene: moderate pCO2
and warm, wet summers caused C4 Chenopodiaceae s.s. and Poaceae to flourish throughout northeastern Tibet (Fig. 4). We use
these boundary conditions to incorporate precipitation into the
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
29
Fig. 4. Qinghai d13Cwax record compared to other climate and environmental reconstructions. A. Qinghai d13Cwax. Maximum summer insolation (gray; Laskar et al., 2004). B. Ages of
glacier maxima in the Dalijia Mountains (J. Wang et al., 2013). C. Atmospheric carbon dioxide concentrations from Antarctic ice cores (Jouzel et al., 2007). D. Mean annual air
temperature on the CLP (Peterse et al., 2011; see SI for calibration details; 1s analytical error is 0.2 C). E. Total organic carbon (TOC) d13C from Weinan and Huanxian loess sections
(Liu et al., 2005) and from Lake Rutundu in Kenya (Wooller et al., 2003), and d13Cwax from Xunyi loess section (Zhang et al., 2003), note different y-axis scales. Inferred C4 abundance
from the original publications (1s analytical error is 0.1e0.3&). F. Speleothem d18O from Sanbao and Hulu caves (Wang et al., 2008). Gray bars as in Fig. 3.
model by Ehleringer et al. (1997) that predicts the CO2 and temperature conditions that favor C3 or C4 plants (Fig. 5, curves
representative for the Tibetan Plateau). The boundary conditions
between C3 and C4 plants calculated by Ehleringer et al. (1997)
cannot explain the changes in C4 plant abundance that we reconstruct at Lake Qinghai. We therefore constructed a schematic representation of the effects of precipitation (Fig. 5). Therein, isohyets
represent dry (ca 100 mm/growing season; Last Glacial), wet
(ca 330 mm/growing season; early Holocene), and moderate precipitation conditions (ca 220 mm/growing season; modern) and
serve as boundaries between conditions that favor C3 and C4 plants.
The isohyets were drawn to have slopes similar to those calculated
by Ehleringer et al. (1997), and were positioned to represent a best
fit to our %C4 plant results. Our results support recent findings that
the conditions that favor C4 plant productivity shift not only in
response to temperature and pCO2, but also in response to growing
season precipitation (Edwards and Still, 2008; Edwards and Smith,
2010).
4.1. Plant ecosystems in the Lake Qinghai catchment during the
glacial period
During the glacial period (32e14 ka), Lake Qinghai d13Cwax
ranged from 34.0 to 22.5&, indicating C3 plants were dominant
(Fig. 3). Overall primary productivity was low from 32 to 15 ka, as
indicated by low pollen counts (Fig. 3) and multiple bulk organic
geochemical proxies (X. Liu et al., 2013). Mean annual temperature
reconstructed on the Chinese Loess Plateau (CLP; Peterse et al.,
2011) and summer temperature at Lake Qinghai in the transient
simulation of the CCSM3 (Z. Liu et al., 2009) were 3e6 C lower than
present (Figs. 2e4, and S2; see SI). Precipitation, reconstructed
using carbonate in Lake Qinghai sediments and simulated by
30
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
Fig. 5. Schematic diagram illustrating environmental conditions (temperature, pCO2
and precipitation) controlling plant ecosystems on the Tibetan Plateau. Increased
precipitation causes C4 plants to be favored under cooler and higher pCO2 conditions,
as shown by isohyets based on data from this paper: wet isohyet (green), moderate
isohyet (gray), dry isohyet (brown). Temperature and pCO2 axes and slopes of isohyet
boundaries based on Ehleringer et al. (1997), and isohyets are drawn to yield a best fit
to our %C4 plant results. “Moderate precipitation” corresponds to 220 mm in summer,
based on modern instrumental data (“China Meteorological Data Sharing Service
System,” 2012; all three conditions are arid: 50% more summer precipitation during
the “wet” early Holocene would be ca 330 mm; 50% less summer precipitation during
the “dry” LGM would be ca 110 mm; Fig. 2). Ellipses indicate conditions at time periods
in the Lake Qinghai d13Cwax record, outline color corresponds to precipitation conditions, fill corresponds to dominant photosynthetic pathway (C3, white; C4, yellow),
ellipses cover the temperature range for that time period based on 20% temperature
amplification at Lake Qinghai relative to the CLP (X. Liu et al., 2009; Peterse et al., 2011;
see SI). Black dots and bars are ranges of projected pCO2 and temperature at Lake
Qinghai in 2040e2059 AD from CMIP5 simulations using emissions scenarios RCP2.6
and RCP8.5 (Taylor et al., 2011). (For interpretation of the references to colour in this
figure legend, the reader is referred to the web version of this article.).
CCSM3, was low throughout the glacial period (Figs. 2 and 3, and
S3; see SI; Z. Liu et al., 2009; An et al., 2012). Although these harsh
conditions were more favorable for C3 plants (Fig. 5), two distinct
intervals exhibit rapid shifts to elevated C4 plant abundance: 21.0e
20.0 ka (average 40%, range 20%e70%) and 17.5e15.8 ka (average
35%, range 25%e60%). We interpret these peaks in d13Cwax as a local
plant community response to changes in lake level during the
coldest and driest portion of the glacial period (23e15 ka; Figs. 3
and 4).
4.1.1. C4 plants may have colonized dry, salty lake beds during the
glacial period
The most likely reason for the large (up to 10&) intermittent
increases in d13Cwax from 21 to 15 ka (Fig. 3) is an increase in C4
plant abundance. This is a surprising finding, however, because the
conditions on the Tibetan Plateau during the glacial period were
extremely cold and dry, inhibiting most primary productivity, and
certainly not favorable to warm-adapted C4 plants (Figs. 3 and 5).
We propose one possible interpretation of these brief d13Cwax increases: Lake Qinghai level dropped during the dry glacial period,
so cold-, salt-, drought-tolerant C4 Chenopodiaceae s.s. colonized
the dry, salty Lake Qinghai bed.
Summer monsoon precipitation was low during the glacial
period, and westerly wind strength decreased starting ca 23 ka
(Fig. 3; An et al., 2012), so total precipitation likely decreased,
causing the Lake Qinghai level to drop. Modeled water balance
(precipitation minus evaporation) was low during maximum
glacial conditions, further evidence for enhanced aridity in the Lake
Qinghai catchment (Fig. 2). Submerged beach ridges and sandy-silt
layers that date to ca 19 ka indicate low levels at Lake Qinghai
(Colman et al., 2007). Aquatic plant pollen is not readily transported
over long distances (Cook, 1988), so the presence of abundant
aquatic plant pollen at the drill site from 21 to 15 ka suggests that
aquatic plants were growing near the drill site (Fig. 3; Ji et al., 2005;
S. Xue, personal communication). These plants generally root in
water that is <7 m deep (Sheldon and Boylen, 1977), so this provides further evidence for lower Lake Qinghai levels. Other records
at Lake Qinghai and elsewhere in Tibet indicate dry conditions and
lower lake levels during the glacial period (Herzschuh et al., 2010;
Mügler et al., 2010; An et al., 2012; X. Liu et al., 2013; Y. Wang et al.,
2013). The Qinghai lake bed did not desiccate completely, however,
as sedimentation was continuous with no evidence for subaerial
exposure at the drill site, located at the depocenter of the lake (An
et al., 2012).
Glacier maxima in the Dalijia Mountains, 220 km southeast of
Lake Qinghai, at 21.8 1.5 ka and 17.3 1.5 ka, are evidence of
maximum cold conditions, corresponding to the lowest temperatures reconstructed on the CLP (Fig. 4; Peterse et al., 2011; J. Wang
et al., 2013). Despite cold and arid conditions, low pCO2 would have
favored C4 plants (Figs. 4 and 5; Jouzel et al., 2007). Chenopodiaceae
s.s. are early succession plants, and C4 photosynthesis is more
abundant in Chenopodiaceae s.s. lineages that exhibit salttolerance and succulence, both of which would have been critical
adaptations to surviving the arid glacial period on the Tibetan
Plateau (Pyankov et al., 2000; Wang, 2007; Kadereit et al., 2012).
Chenopodiaceae s.s. pollen was abundant (20e40%) during the
glacial d13Cwax peaks (Fig. 3; Ji et al., 2005; S. Xue, personal
communication). We hypothesize that C4 Chenopodiaceae s.s.
colonized the exposed, salty lake bed when Lake Qinghai levels
dropped during the glacial period. This increase in C4 Chenopodiaceae s.s. would have been a local phenomenon, constrained to
exposed lake beds (Fig. S1). This hypothesis can be tested in future
studies: other desiccated lake beds may also show intermittent
increases in d13Cwax, whereas terrestrial sediment deposits (e.g.,
loess) on the Tibetan Plateau would not contain evidence for these
d13Cwax increases.
4.2. Transition to the Lateglacial period
At ca 16 ka, the westerly winds strengthened, likely in response
to Heinrich Event 1 (H1; Sun et al., 2011; An et al., 2012). From 16 to
14.5 ka, tree pollen increased in abundance and d13Cwax decreased,
indicating that C3 plants dominated during H1 (Fig. 3; Ji et al.,
2005). Immediately following H1, d13Cwax increased, but returned
to consistently low values (32&) from 14.5 to 13.7 ka. Artemisia
represented 80% of pollen from 14.5 to 13.7 ka, which would
explain the strong C3 plant signal in d13Cwax. Other proxies indicate
increasing temperature, increasing summer precipitation, and
increasing seasonal insolation contrast during this time period
(Figs. 3 and 4, and S4), so it is unclear why the d13Cwax and pollen
suggest stable ecological conditions from 14.5 to 13.7 ka.
4.3. C4 plants were abundant on the Tibetan Plateau during the
Lateglacial and early Holocene
During the Lateglacial and early Holocene (13.7e8.3 ka), Lake
Qinghai d13Cwax ranged from 29.5 to 21.8&, corresponding to an
average of 50% C4 plants (Fig. 3). We hypothesize that this increase
in C4 plant abundance was caused by a combination of environmental changes: high seasonal insolation contrast, moderate pCO2
and warm conditions, and greater summer precipitation.
Winter insolation was low and summer insolation was high at
Lake Qinghai during the early Holocene, resulting in a seasonal
insolation contrast of ca 350 W m2 (Fig. S4; Laskar et al., 2004).
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
Cold winters and springs likely inhibited C3 plant growth, whereas
short, hot, wet summers favored C4 plant productivity (Ehleringer
et al., 1997; Pyankov et al., 2000). Global pCO2 was 240e
260 ppmv (Jouzel et al., 2007), values that favor C4 photosynthesis
only at higher temperatures (Fig. 5; Ehleringer et al., 1997). Lateglacial and early Holocene temperature was 1e3 C higher than
present, according to a pollen record from Lake Luanhaizi in the
nearby Qilian mountains, the CCSM3 transient simulation, and the
temperature reconstruction on the CLP (Figs. 2 and 4; Z. Liu et al.,
2009; Herzschuh et al., 2010; Peterse et al., 2011). Precipitation
increased from 13.7 to 12 ka and peaked 12 to 8 ka, according to
d18Oostracode from Lake Qinghai, the pollen record from Lake Luanhaizi, and the CCSM3 transient simulation (Figs. 2e4; Liu et al.,
2007; Z. Liu et al., 2009; Herzschuh et al., 2010; An et al., 2012).
Higher lake levels, suggesting wetter conditions, existed
throughout Tibet during the early Holocene, including at Lake
Donggi Cona, 200 km southwest of Lake Qinghai (Dietze et al.,
2013; Hudson and Quade, 2013).
Warmer conditions were favorable for primary production, as
indicated by increased pollen flux at ca 14.8 ka and multiple bulk
organic geochemical proxies from Lake Qinghai (Fig. 3; An et al.,
2012; X. Liu et al., 2013). Poaceae and Chenopodiaceae s.s. each
composed 10e20% of total pollen flux during the Lateglacial and
early Holocene, Chenopodiaceae s.s. pollen increased slightly during the Younger Dryas (Fig. 3; Ji et al., 2005). Tree pollen decreased
to 10% during the Younger Dryas, and increased abruptly to 20% at
the end of the Younger Dryas, when total pollen counts also
increased. Although the existing data do not distinguish C3 from C4
plant pollen, the 10& increase in d13Cwax cannot be explained by
changes in C3 plant water stress, and so C4 plants must have
flourished during the Lateglacial and early Holocene. Relatively
warm, wet conditions, occurring at a time of maximum seasonal
contrast during the Lateglacial and early Holocene, would be
favorable to both C4 Poaceae and C4 Chenopodiaceae s.s. This increase in C4 plant abundance may have resulted from a few extant
taxa that proliferated on the QinghaieTibetan Plateau during this
period, or may have resulted from C4 plant species shifting to
higher elevations as climate became more conducive to their
growth (Fig. S1). In either case, the Lateglacial and early Holocene
increase in C4 plant abundance was driven by regional and global
environmental conditions, and therefore C4 plants were likely
dominant throughout the region around Lake Qinghai.
4.4. Mid-Holocene development of a C3-plant-dominated
ecosystem
The mid-Holocene d13Cwax decrease is mirrored by decreasing
bulk organic matter d13C (X. Liu et al., 2013). Aquatic plants exert
only a minimal influence on d13Cwax, so we can more confidently
conclude that this decrease in carbon isotope values is due to a
decrease in C4 plant biomass. The initial decline of C4 plants during
the mid-Holocene (8e6 ka) coincided with high counts of tree
pollen, as well as decreasing precipitation and insolation, as well as
decreasing seasonal contrast (Figs. 2e4, and S4; Laskar et al., 2004;
Ji et al., 2005; Peterse et al., 2011; An et al., 2012). C3 plants
dominated the Lake Qinghai catchment after ca 6 ka, coincident
with high pCO2 and modeled increasing May temperatures and
winter precipitation, which favored C3 plant productivity (Figs. 2e
4; Still et al., 2003). Whereas arboreal pollen declined during the
late Holocene, likely due to decreased precipitation (Herzschuh
et al., 2009), Chenopodiaceae s.s. and Poaceae remained constant,
suggesting that C3 plants within these clades became dominant,
replacing C4 Chenopodiaceae s.s. and Poaceae that had dominated
during the early Holocene (Fig. 3). Today, high pCO2 means that
most C4 plant communities are near the edge of their ecological
31
niche, especially those in cold regions (Fig. 5). The predicted 2e3 C
temperature increase on the Tibetan Plateau by 2050 AD will not be
sufficient to offset the deleterious effects of 450e500 ppmv CO2,
likely resulting in the demise of C4 plants in cold, dry, highelevation regions (Fig. 5; Taylor et al., 2011).
4.5. C4 plants in high-elevation ecosystems
In contrast to the northeastern Tibetan Plateau, high-elevation
sites in equatorial Africa and South America hosted flourishing C4
plant communities during the glacial period. The different timing of
maximum C4 plant abundance is likely due to different temperatures and seasonal contrasts. The equatorial sites had higher mean
annual temperatures than the northeastern Tibetan Plateau during
the glacial period (Figs. 4 and S4). Seasonal insolation contrast is
minimal at the equator, ranging from 40 to 60 W m2, with minimum insolation contrast occurring during the glacial period when
there were maximum C4 plants (Fig. S4; Berger et al., 2006). Thus,
seasonal insolation contrast may not play a dominant role in plant
ecosystem variability at the equator. Instead C4 plants flourished
during the glacial period likely due to sufficiently warm rainy
seasons and low pCO2 (Figs. 4 and S4; Jouzel et al., 2007; Loomis
et al., 2012).
At latitudes similar to Lake Qinghai but at lower elevation on the
CLP, C4 plants rarely exceeded 40% abundance. Despite their relatively low abundance, C4 plants persisted on the CLP until the late
Holocene, perhaps due to warmer, wetter summers (Fig. 4; Zhang
et al., 2003; Liu et al., 2005).
5. Conclusions
Our paleoecological data demonstrate that C4 plants can thrive
on the Tibetan Plateau, and provide benchmarks for ecosystem
models that infer <0.5% C4 plants on the Tibetan Plateau today. The
CCSM3 transient simulation infers 0% C4 grasses even during time
periods when Lake Qinghai d13Cwax suggests up to 50% C4 plants
(Figs. 1 and 3, and S5; Still et al., 2003; Z. Liu et al., 2009). Although
we have evidence for abundant C4 plant biomass around Lake
Qinghai during the glacial period, it will be most important to
correctly model the increase in C4 plant abundance during the
Lateglacial and early Holocene, which was likely a more widespread
phenomenon. Arid- and cold-adapted Chenopodiaceae s.s. likely
evolved C4 photosynthesis as a further adaptation to cold, dry, salty
conditions on the Tibetan Plateau (Kadereit et al., 2012), and
therefore do not fit with the warm, wet thresholds for C4 plants that
are currently incorporated into ecosystem models (Collatz et al.,
1998; Still et al., 2003). As the spatial resolution of climate and
ecosystem models increases, it will be necessary to account for
unusual ecosystem dynamics, including cold-, arid-, salt-adapted
C4 Chenopodiaceae s.s., in spatially heterogenous, high-elevation
regions.
The combination of saline soils, high irradiance, and summerfocused precipitation on the Tibetan Plateau inherently favor C4
plants, whereas cool conditions and high pCO2 favor C3 plants. A
delicate ecological balance therefore exists on the Tibetan Plateau
and in other high-elevation regions, where we document large
paleoecological transitions between C3 and C4 plants. Lake Qinghai
d13Cwax provides a paleoecological perspective for studies of modern distributions of C4 plants, which find that temperature, precipitation, and pCO2 all play important roles (Ehleringer et al., 1997;
Collatz et al., 1998; Sage et al., 1999; Edwards and Smith, 2010;
Kadereit et al., 2012). Due to relatively high pCO2 today, C4 plant
communities in cold, dry, high-elevation regions are at the edge of
their ecological niche, and will likely decline further as pCO2 increases (Taylor et al., 2011).
32
E.K. Thomas et al. / Quaternary Science Reviews 87 (2014) 24e33
Author contributions
YH designed the study; EKT, JZ, PW, and LG performed sample
preparation and analysis; EKT, YH, SMC, and SCC performed data
analysis and interpretation; CM provided model output and analysis; EKT wrote the main paper and the Supplementary Information, with input from YH, CM, SMC, and SCC.
Acknowledgments
We thank R. Tarozo for lab assistance and E. J. Edwards and one
anonymous reviewer for providing feedback on the manuscript. We
thank the International Continental Scientific Drilling Program, the
United States National Science Foundation, the National Natural
Science Foundation of China and the Ministry of Science and
Technology of China for their support for the Lake Qinghai Drilling
Project, which was led in part by A. Zhisheng. We thank Z. Liu and B.
Otto-Bliesner for sharing CCSM3 output. The CCSM3 transient
simulation is supported by the P2C2 program at the US National
Science Foundation, the Abrupt Change Program, EaSM program,
and INCITE computing program at the US Department of Energy,
and NCAR. We acknowledge the World Climate Research Programme’s Working Group on Coupled Modelling, which is
responsible for CMIP, and we thank the climate modeling groups
(listed in Table S1) for producing and making available their model
output. For CMIP the U.S. Department of Energy’s Program for
Climate Model Diagnosis and Intercomparison provides coordinating support and led development of software infrastructure in
partnership with the Global Organization for Earth System Science
Portals. This research was funded by NSF grant #ATM-0902805 to Y.
Huang and a NSF Graduate Research Fellowship to EKT.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.quascirev.2013.12.014.
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