Forest contraction in north equatorial Southeast Asia during the Last Glacial Period

Abstract

Today, insular Southeast Asia is important for both its remarkably rich biodiversity and globally significant roles in atmospheric and oceanic circulation. Despite the fundamental importance of environmental history for diversity and conservation, there is little primary evidence concerning the nature of vegetation in north equatorial Southeast Asia during the Last Glacial Period (LGP). As a result, even the general distribution of vegetation during the Last Glacial Maximum is debated. Here we show, using the stable carbon isotope composition of ancient cave guano profiles, that there was a substantial forest contraction during the LGP on both peninsular Malaysia and Palawan, while rainforest was maintained in northern Borneo. These results directly support rainforest "refugia" hypotheses and provide evidence that environmental barriers likely reduced genetic mixing between Borneo and Sumatra flora and fauna. Moreover, it sheds light on possible early human dispersal events.

Full text

Forest contraction in north equatorial Southeast Asia
during the Last Glacial Period
Christopher M. Wurster
a,1,2
, Michael I. Bird
b
, Ian D. Bull
c
, Frances Creed
c
, Charlotte Bryant
d
, Jennifer A. J. Dungait
c,3
,
and Victor Paz
e
a
School of Geography and Geosciences, University of St. Andrews, St. Andrews, Fife KY16 9AL, United Kingdom;
b
School of Earth and Environmental Sciences,
James Cook University, Cairns, QLD 4870, Australia;
c
Organic Geochemistry Unit, Bristol Biogeochemistry Research Centre, School of Chemistry, University of
Bristol, Cantock’s Close, Bristol BS8 1TS, United Kingdom;
d
Natural Environment Research Council, Radiocarbon Laboratory, East Kilbride G75 OQF, United
Kingdom; and
e
Archaeological Studies Program, University of the Philippines, Diliman, Quezon City 1101, Philippines
Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved July 9, 2010 (received for review April 22, 2010)
Today, insular Southeast Asia is important for both its remarkably
rich biodiversity and globally significant roles in atmospheric and
oceanic circulation. Despite the fundamental importance of envi-
ronmental history for diversity and conservation, there is little
primary evidence concerning the nature of vegetation in north
equatorial Southeast Asia during the Last Glacial Period (LGP). As
a result, even the general distribution of vegetation during the Last
Glacial Maximum is debated. Here we show, using the stable
carbon isotope composition of ancient cave guano profiles, that
there was a substantial forest contraction during the LGP on both
peninsular Malaysia and Palawan, while rainforest was maintained
in northern Borneo. These results directly support rainforest “re-
fugia”hypotheses and provide evidence that environmental bar-
riers likely reduced genetic mixing between Borneo and Sumatra
flora and fauna. Moreover, it sheds light on possible early human
dispersal events.
biogeography
|
paleoecology
|
refugia
|
stable isotope
|
Sundaland
Equatorial Southeast Asia contains many unique endemics that
contribute to the region’s designation as a “biodiversity”
hotspot, and understanding the region’s environmental history
bears directly on conservation issues (1–3). Its rich flora and fauna
(20–25% of plant and animal species despite its small land area) is
not solely a result of contemporary patterns in ecology and en-
vironment; perhaps no other region in the world bears such
a strong imprint of historical environmental change on its present
biogeography (3). Contemporary humid tropical conditions of
insular Southeast Asia are maintained by the seasonal reversal of
winds that bring the East Asian (northeast) and Australasian
(southwest) monsoon systems. The shallow seas surrounding the
submerged Sunda shelf are part of the Indo-Pacific Warm Pool
(IPWP), among the warmest and wettest on Earth, playing several
key roles in global atmospheric and oceanic circulation (4). The
IPWP is an area where sea surface temperatures remain above
28 °C and precipitation excess is high due to monsoonal activity
(4). As a result, it is globally important as a source of latent heat
and moisture for global atmospheric circulation, and for its role in
energy transfer between the Pacific and Indian oceans (5).
Moreover, the region plays a key role in El Niño-Southern Os-
cillation dynamics (5).
During the Last Glacial Period (LGP; 125–10 kiloyear [kyr]
ago), particularly the Last Glacial Maximum (LGM; 23–19 kyr
ago), reduced global sea level exposed the continental shelf from
south of Thailand to Sumatra, Java, and Borneo, revealing the
contiguous continent Sundaland (6), with a land area the size of
Europe. Oceanic temperatures surrounding Sundaland during
the LGM were 2–3 °C cooler than today, and foraminiferal δ
18
O
values are interpreted to reflect reduced precipitation (5).
Inferred environments on the exposed landmass are a conten-
tious issue, particularly north of the equator, due to the paucity
of well-dated proxy information from the LGM (6–8). It has
been hypothesized that forest was replaced by savanna over
large areas (9, 10) or, alternatively, that lowland tropical rain-
forest persisted despite any reduction in rainfall (8, 11). In ad-
dition, model results for the region greatly vary, with some
indicating that a broad continuous lowland tropical rainforest
was maintained and others suggesting savanna over major por-
tions of Sundaland during the LGM (6, 7). Surprisingly, there
are no records from peninsular Malaysia and, in places where
LGM sediments with suitable proxies are recovered, they may be
compromised by biases such as riparian gallery forest vegetation
and wind-blown tree pollen dominating riverine and offshore
deposits (6, 8, 11, 12), or lowland swamp regions being biased
toward indicating wetter conditions (13). Hence, even the gen-
eral distribution of LGM vegetation is disputed.
An overlooked terrestrial depositional record exists in caves that
serve as roosts to swiftlets (Aerodramus sp.) and/or insectivorous
bats. Over time, their feces (guano) accumulate in deposits several
meters thick, representing a time-transgressive proxy record
amenable to radiocarbon dating (14). Fresh guano is composed
dominantly of finely comminuted insect cuticles that are sub-
sequently broken down by bacteria and fungi. Interactions with
drip water, cave material, and guano lead to the formation of
unique guano-specific phosphate and nitrogen minerals in an
earthy organic matrix (15). These sediments contain multiproxy
information from a variety of sources including the stable isotope
composition of various extractable organic materials. Herein we
use results obtained from δ
13
C analyses of insect cuticles and
molecular δ
13
C analyses of normal alkanes (n-alkanes), both
extracted from four guano deposits in northern Sundaland, to infer
local vegetation changes during the LGP. Caverniculous bats and
birds feed within a limited area of the roost and are nonspecificin
their predation of insects (16), which in turn are as abundant as
their plant hosts (17). In lowland tropical locations, grasses use the
C
4
photosynthetic pathway, whereas trees use the C
3
pathway. The
different enzymatic pathways of fixing CO
2
result in δ
13
C values of
C
4
plants [−9to−16‰(per mille)] and their insect hosts that are
substantially different from those of C
3
plants (−19 to −34‰) (18).
This apparently large range in δ
13
C values is considerably reduced
at the biome level (19). Therefore, an integrated measure of the
δ
13
C values of insect carapaces will directly reflect the relative
abundance of C
4
vegetation in a region (16), and variation in insect
Author contributions: C.M.W., M.I.B., andI.D.B. designed research; C.M.W., M.I.B.,F.C., C.B.,
J.A.J.D., and V.P. performed research; I.D.B. contributed new reagents/analytic tools;
C.M.W., M.I.B., I.D.B., and C.B. analyzed data; and C.M.W. and M.I.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed at the present address. E-mail: christopher.
wurster@jcu.edu.au.
2
Present address: School of Earth and Environmental Sciences, James Cook University, P.O.
Box 6811, Cairns, QLD 4870, Australia.
3
Present address: North Wyke Research, Okehampton, Devon EX20 2SB, United Kingdom.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1005507107/-/DCSupplemental.
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cuticular δ
13
C values within a cave guano deposit will un-
ambiguously reflect changes in the abundance of C
4
relative to C
3
vegetation in the region surrounding the cave (16, 20).
Insular Southeast Asia is rich in Karst terranes that house
large populations of insectivorous bats and swiftlets. Although
some cave sites are roosts to relatively large populations of fruit
bats, we limited our selection to those with insectivorous colo-
nies. Extraction of insect cuticles from the guano sediment, pH,
and C:N ratios confirmed that insectivorous populations
remained dominant throughout each record. We located four
sites with LGM sediment deposition within ∼10° north of the
equator (Fig. 1). Along a transect from west to east are deposits
in Batu cave (3°13′N, 101°42′E) near Kuala Lumpur in penin-
sular Malaysia; Niah cave (3°49′N, 113°46′E) in Sarawak, north-
ern Borneo, and two sites in Palawan, Philippines, Gangub cave
(8°31′N, 117°33′E) in the south and Makangit cave (10°28′N,
119°27′E) in the north. Age control is provided by radiocarbon
dates on insect cuticles (14) taken from discrete intervals through
each guano sequence, one charcoal sample from the Batu de-
posit, and three solvent-extracted bulk guano samples. Radio-
carbon dates were calibrated to calendar years using the IntCal09
calibration curve (21) implemented using OXCAL 4.1 (22)
(Tables S1,S2, and Fig. S1).
Results
The δ
13
C profile from the Batu deposit indicates that C
4
biomass
was a significant component of regional vegetation from at least
35 until 16 kyr ago, with values remaining above −22.6‰until the
end of the LGM (SI Text provides information on C
4
production
estimates). After the LGM, an initial decline in δ
13
C values oc-
curred at ∼14.7 kyr ago, with an increase in δ
13
C values to −23.3‰
occurring between 13.4 and 12.5 kyr ago. Dominantly C
3
(forest)
values (−26‰) are evident after 10.5 kyr ago and persisted until
the present (Fig. 2). In the Niah deposit, Holocene sediment is
missing due to mining of the upper part of the sequence for fer-
tilizer, but δ
13
C values of insect cuticles from ∼50–10.7 kyr ago
indicate that C
3
-dominant vegetation persisted through the LGM,
with δ
13
C values consistently between −24.7 and −26.2‰, aside
from a brief increase to −22.9‰at ∼13.4 kyr ago. Both records
from Palawan show the clearest example of forest collapse during the LGM. Gangub cave has δ
13
C values indicative of Pleistocene
forest until ∼33.5 kyr ago, after which time a substantial increase
in δ
13
C values occurred, from −26 to −18‰at 21 kyr ago, in-
dicative of open savanna (C
4
) vegetation. Rainforest was again
present in the cave area by 13.5 kyr ago. Makangit guano sediment
contained lithogenic graphite, making it difficult to extract and
analyze insect cuticles directly. To circumvent this problem, n-
alkanes were extracted and compound-specificδ
13
C values were
determined (SI Text provides background information). Normal
alkanes with a strong odd-over-even predominance represent
epicuticular waxes, and are a direct biomarker of terrestrial veg-
etation (23, 24). As with the Gangub profile, the C
29
and C
31
n-
alkanes exhibit relatively low δ
13
C values suggesting rainforest
at ∼50 kyr ago, with highest values occurring during the LGM.
The C
29
n-alkane reaches maximum values of −19.5‰beginning
around 23 kyr ago. These high values declined after the LGM and
by 8 kyr ago are −28.6‰, showing a return of forest vegetation. By
the mid-Holocene, δ
13
C values are as low as −30.3‰, and con-
tinued to be low until the present. Two increases in δ
13
C values
punctuated this overall decline, dated at 13.1 and 9.7 kyr ago. An
analogous trend is also observed by plotting an n-alkane abun-
dance ratio (n-C
29
/n-C
31
), the changes being derived directly from
an input of epicuticular waxes from different plant species with
time (23) (Fig. S2).
Discussion
Forest Contraction in Northern Sundaland. There are few well-dated
LGM records from Sundaland, leading to the use of modern
Fig. 1. Map of Southeast Asia showing the land–sea distribution during the
Last Glacial Maximum estimated from the 120-m bathymetric line. A dashed
line indicates the 50-m bathymetric line, which is a better representation of
land–sea distribution at the time of human migration into the region. Study
sites are displayed, where solid black (white) indicates evidence for forest
(open) conditions during the LGM. The diamond represents the site location
of a speleothem record (34). Earlier proposed savanna (9) and rainforest
refugia (10) are indicated by light gray and dark gray shading. Solid lines
indicate contemporary tropical lowland forest distribution.
Fig. 2. δ
13
Cprofiles of four guano deposits. We measured δ
13
C values of
insect cuticles for Batu (blue closed circles), Niah (green open circles), and
Gangub (red closed circles). For the Makangit profile, lithogenic graphite
contamination significantly affected results and could not be completely
removed, so we measured δ
13
C values of individual C
29
(closed) and C
31
(open) n-alkanes (orange diamonds). Although δ
13
C values of n-alkanes are
not directly analogous to those of insect cuticles, both are related to C
4
and
C
3
relative abundances (SI Text). We also plot speleothem δ
18
O values from
Gunung Buda National Park (34), and mark the LGM and a period of reduced
precipitation at 14.2 ±0.2 kyr ago. For direct comparison, equivalent scales
are used for δ
13
C axes. Radiocarbon measurements are from insect cuticles,
except for one charcoal sample and three solvent-extracted guano samples
(Tables S1 and S2 and Fig. S1). VPDB, Vienna Pee Dee Belemnite; VSMOW,
Vienna standard mean ocean water.
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biogeographic patterns and undated geomorphic evidence and
even lack of evidence to interpret general vegetation distribution
(6), much of which remains is conflicting (1). The southern
portion has considerably more information than north of the
equator. Taken together, there are either conflicting inter-
pretations or complete lack of information for more areas than
for those where there is substantial agreement. This study un-
equivocally demonstrates that savanna expanded in the Sunda-
land region north of the equator, by at least 400 km on peninsular
Malaysia, and was an important contributor to plant biomass
(Table S3,SI Text, and Fig. S3). A recent vegetation model for the
region found that a continuous belt of lowland tropical rainforest
should have persisted (7), and this conclusion is supported by
pollen analysis of LGM river and offshore sediments from the
South China Sea (8, 11). However, an increasing number of ge-
netic studies show that migration between Sumatra and Borneo
was extremely limited during the LGP even though the major is-
lands were connected for most of the last 70 kyr (25–29), and
possible rainforest refugia were inferred using termite morphol-
ogy and taxonomic groupings (10), which worked well with other
estimates derived from vicariant murine rodents (27). A savanna
vegetation barrier such as we interpreted from the Batu δ
13
C
profile can explain such limited crossover of rainforest specialists
between east and west Sundaland.
Extant rainforest-dependent species on Palawan today have
been argued to suggest that forest persisted on the island during
the LGM (12), whereas we infer open savanna conditions. Al-
though a preliminary record from Palawan found savanna was
present during the LGP on the north of the island (30), the in-
terpretation of this record suffered from having only two radio-
carbon dates and the presence of lithogenic graphite contami-
nation. Nonetheless, some argued that the southern portion must
have been forested and could have served as refugia (1, 7). We
show using the guano profiles from Makangit and Gangub that
both the north and south of Palawan were opensavanna during the
LGM and any rainforest refugia on the island must have been
severely reduced. For example, this highly mountainous region
may have provided refugia at higher elevation for forest specialists
(31). It is likely that Palawan was not connected to Borneo during
the LGM (32), and rainforest specialists would have derived from
an earlier time. Other evidence from Niah cave suggests that forest
cover was maintained in northern Borneo from at least 40 kyr ago
(2, 33), and this is in agreement with our results.
Brief savanna re-expansions after the LGM apparent in guano
δ
13
C values in northern Palawan at 9.7 kyr ago and southern
Palawan at 4.7 kyr ago may be due to local changes (e.g., human
clearance), but increased δ
13
C values occurred ∼13.4 kyr ago at all
locations except Gangub, suggesting a more regional climate-
induced vegetation response at this time. A δ
18
O profile from Mulu
cave speleothems, Sarawak, indicates a drier period centered at
13.0 ±0.2 kyr ago coincident with the Antarctic Cold Reversal,
which interrupted an increasing trend in precipitation (34). Such
a decrease in rainfall could be responsible for a short phase of
forest contraction at this time, as indicated in the guano record.
Environments of Early Human Dispersal. Our results also provide
fundamental evidence for understanding patterns of early human
dispersal into the region. A major modern human expansion
occurred in Southeast Asia at ∼60–40 kyr ago (35), possibly
during a time of relatively mild climate and stable shorelines
favoring coastal exploitation (36). We infer an environmental
backdrop for Sundaland during the LGP that indicates a sub-
stantial area of savanna covered Sundaland north of the equator,
potentially facilitating human dispersal through the region. This
may have limited the area of tropical forest to be traversed to
occupy Niah cave by 46 kyr ago (33). Although early humans
could evidently deal with rainforest habitat at Niah, possibly with
the aid of fire (33), dispersal over more familiar open woodland
or savanna habitats through the core of Sundaland, followed by
movement along the coast, provides an alternate scenario for
human migration into Sundaland that does not require pene-
tration of large areas of dense tropical rainforest.
Methods
All deposits were sampled from pits excavated through the accumulated
guano. Exposed profiles were sampled at 3- to 5-cm intervals, adjusted where
necessaryto ensure that sample intervalsdid not cross stratigraphic boundaries.
Sampleswere kept in a cold store at 4 °C until freeze-dried.A detailed extraction
procedure has been previouslydescribed for the recovery of insect cuticles from
guano sediment (37). Approximately 250–300μg of sample was placed into tin
capsules and δ
13
C values were measured using a Costech elemental analyzer
fitted with a zero-blank autosampler coupled via a ConFloIII interfaced with a
Thermo Finnigan DeltaPlus-XL isotope ratio mass spectrometer at the Univer-
sity of St Andrews Facility for Earth and Environmental Analysis. International
Atomic Energy Agency-issued and internal reference materials were run
alongside samples to normalize δ
13
C values to the Vienna Pee Dee Belemnite
(VPDB) reference scale and monitor instrument performance. All data are
reported in per mille (‰) deviations from the VPDB-normalized reference
standard scale. Reproducibility (SD) of three or four replicates of an internal
laboratory reference material (processed from desert bat guano fertilizer)
measured within each run of ∼30 samples was within ±0.2‰.
Normal alkane fractions were extracted from guano, isolated, and then
analyzed by gas chromatography (GC) (24). GC combustion isotope ratio mass
spectrometry (GC/C/IRMS) analyses were made on 1.0 mL-aliquots using
a Varian 3400 gas chromatograph fitted with a septum-equipped temper-
ature programmable injector (SPI); the analytical column and temperature
program used were the same as those used for the GC analyses. This was
coupled to a Finnigan MAT Delta S stable isotope mass spectrometer.
Age models for each profile were constructed using radiocarbon meas-
urements calibrated to calendar years using IntCal09 (21) implemented using
OXCAL 4.1 (22). Calendar year as a function of depth was determined using
point-to-point linear interpolation using a mean calendar age and associated
2σconfidence limit determined using the OXCAL program and based on the
probability distribution of calibrated ages for a given radiocarbon age and
depth midpoint. Sediment deposition rate is similar among deposits (Fig. S1).
Extraction methods have been previously described (14, 37). Niah cave is
missing Holocene sediment due to recent guano mining. Radiocarbon dates
of extracted insect cuticles were prepared at the NERC Radiocarbon Facility
and measured at the Scottish Universities Environmental Research Centre
Accelerator Mass Spectrometry facility, East Kilbride, Scotland. In the deposit
from Makangit, lithogenic graphite affected the
14
C result, necessitating
correction before calibration (Table S2).
ACKNOWLEDGMENTS. We thank A. Calder for help in the laboratory, and
M. Zimmermann, G. Saiz, and P. Ascough for useful discussions. This study
was supported by NERC Standard Grant NE/D001501 with in-kind support
from NERC Radiocarbon Facilities (allocations 1067.0404, 1286.0408, 1367.1008).
We also acknowledge the NERC for funding of the mass spectrometry facilities
at Bristol (Contract R8/H12/15).
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