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Journal of Anthropological Archaeology 22 (2003) 292–304
www.elsevier.com/locate/jaa
Neolithic subsistence patterns in northern
Borneo reconstructed with stable carbon isotopes of enamel
John Krigbaum*
Department of Anthropology, University of Florida, 1112 Turlington Hall, Gainesville, FL 32611-7305, USA
Abstract
The Neolithic period in island Southeast Asia is characterized by various population movements, technological
innovations, and the introduction/adoption of agricultural foodstuﬀs. Human subsistence trends during this period,
however, are poorly understood. Broad spectrum foraging is generally assumed for prehistoric groups utilizing rain
forest food resources but the degree to which cultigens were part of the dietary repertoire remains unclear. This paper
explores human subsistence patterns at three penecontemporaneous Neolithic sites in Sarawak (East Malaysia) using
stable isotope ratios of carbon and oxygen derived from tooth enamel apatite. The sites (Niah Cave, Lubang Angin,
and Gua Sireh) diﬀer in local ecology and cultural circumstance but all are situated in C3 -dominant lowland primary
rain forest. Signiﬁcant diﬀerences in d13 C values between sites likely reﬂect the canopy eﬀect and variations in foraging
pattern. Lower values at Lubang Angin suggest dependence upon closed forest foraging. Higher values at Neolithic
Niah Cave and Gua Sireh suggest more open forest horticulture and subsistence, including some form of systematic
food production, collection, and/or habitat modiﬁcation.
Ó 2003 Elsevier Inc. All rights reserved.
Keywords: Southeast Asia; Borneo; Neolithic; Austronesian prehistory; Bioarchaeology; Paleodiet; Bone chemistry; Canopy eﬀect;
Carbon isotopes; Oxygen isotopes
Introduction
The onset of the Neolithic in island Southeast Asia
ca. 4000 years BP is characterized by a complex series of
population movements, cultural and technological innovations, and the introduction of agricultural foodstuﬀs (Bellwood, 1997; Spriggs, 1989). Further evidence
of change during this period is indicated by an increased
frequency of archaeological sites, most commonly found
in caves and rock shelters (Anderson, 1997). Yet despite
the fair number of Neolithic sites in the region, surprisingly little has been done to elucidate dietary trends
during this important period, particularly in the perhumid tropics. To counter this trend, human paleodiet is
*
Fax: 1-352-392-6929.
E-mail address: krigbaum@uﬂ.edu.
directly assessed using stable carbon isotope data derived from human tooth enamel from three Neolithic
sites in northern Borneo. Sites include Niah Cave (West
Mouth), Gua Sireh, and Lubang Angin—all situated in
the East Malaysian state of Sarawak (Fig. 1).
Rain forest diet in prehistory can be viewed as
eclectic in nature but such inferences are based mainly
on supposition, rather than on associated ﬂoral and
faunal evidence. Paleodiet approaches using stable carbon isotopes provides a fresh approach to explore prehistoric human subsistence patterns of tropical foraging
populations in Southeast Asia, where other more traditional methods have proved inadequate. However, reconstructing diet using bones and tooth dentine from
hot and humid environments is often hampered by poor
preservation. Bone may be intact, but too often collagen
is not preserved (e.g., Ambrose, 1990; Ambrose and
Norr, 1992; Pate, 1997). Although the organic collagen
fraction provides more biogeochemical signals to work
0278-4165/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved.
doi:10.1016/S0278-4165(03)00041-2
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
293
Fig. 1. Map of Sarawak (East Malaysia) showing location of Neolithic sites included in this study.
with (namely carbon and nitrogen isotopes), the absence
of collagen limits isotopic study to carbon and oxygen
(and strontium) of the inorganic, apatite portion of bone
and teeth. Krueger and Sullivan (1984) demonstrated
bone apatite carbonate accurately reﬂects the carbon
isotope ratios of the diet. Bone apatite, however, is easily
altered by postmortem diagenesis (Koch et al., 1994;
Lee-Thorp and van der Merwe, 1991; Schoeninger et al.,
1989). Tooth enamel, by contrast, is much more resistant to diagenesis (Wang and Cerling, 1994). The stable
carbon isotope ratio derived from enamel provides a
dietary ÔsignatureÕ of an individualÕs total food intake
during the time of enamel formation, while those of
bone collagen are biased toward the protein fraction of
diet (Ambrose and Norr, 1993; Tieszen and Fagre,
1993). Because of its stability, tooth enamel apatite is the
preferred material in paleodiet studies of vertebrate
fossil remains (e.g., Kingston et al., 1994; Lee-Thorp,
2000; MacFadden, 2000; Quade et al., 1995).
Prehistoric context
The onset and adoption of agriculture by the earlymid Holocene in Southeast Asia fundamentally changed
the cultural and ecological landscape. This transition
from foraging to farming is certainly one of the most
important behavioral advances in human prehistory
(e.g., Harris, 1996). On mainland eastern Asia, the
adoption of plant and animal domesticates into the
subsistence regime occurred over a period of several
millennia in localized centers along the Yangtze and
Yellow River valleys (Glover and Higham, 1996; Higham, 1995; Lu, 1999). Here, foragers responding to an
improving climate after the cooler Younger Dryas (ca.
11,000 years BP) began to transform their landscape and
change their dietary pattern.
To the south in the zone of the humid tropics,
however, the forager-farmer transition is less well documented, and does not seem to have been so culturally
revolutionary. There are very few pre-Neolithic sites
from the lowland tropics that document pre-agricultural
foraging economy. Further, at slightly more numerous
Neolithic sites, it is not always clear what mode of
subsistence is present based on materials recovered in
the archaeological record. Rather, subsistence is more
typically inferred based on associated faunal remains
and artifacts. For example, the presence of earthenware
pottery and ground stone tools tends to be identiﬁed
with the Neolithic and thereby connotes potential presence of food production and increased sedentism. In
part, this lack of subsistence data is a result of poor
preservation of organic remains. It has therefore proved
diﬃcult to assess subsistence systems with any degree of
conﬁdence based on negative evidence and traditional
archaeological techniques.
294
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
The development and adoption of the Neolithic in
island Southeast Asia—its pattern and pulse—is a debated topic. The dominant paradigm is that championed
by Bellwood (1996, 1997) whereby large-scale migration
events of Austronesian-speaking peoples from a Taiwan
homeland (ultimately from South China) branch out
across wide tracts of island Southeast Asia, parts of
Melanesia and on to Polynesia to the East and Southwest to Madagascar. Central to this diﬀusion hypothesis
is a strong linguistic connection (Blust, 1995) centered
on relationships between elements of proto-Austronesian coupled with elements of material culture and food
production (Bellwood, 1997). Meachem (1984) and
others (Oppenheimer, 1998; Solheim, 1996) argue
against diﬀusion and for local evolution events with the
adoption of material culture/agriculture rather than
simply biological/cultural replacement via a major migration event.
With respect to Borneo, one central concern regarding early Austronesian presence is the extent to which
systematic food production was introduced. The climate
of northern Borneo is tropical and perhumid, in contrast
to more northern subtropical (monsoonal) areas where
rice/millet food production originated. Another conundrum concerns the ethnogenesis of the Penan and related groups of extant hunter-gatherers (Brosius, 1991;
Sellato, 1994). If Austronesians arrived Ôfully loadedÕ
with agriculture, and there were no pre-Austronesian
people present on Borneo, then forest hunting and
gathering adaptations would be a secondary adaptation—as Hoﬀman (1986) states, they would be a product
of devolution, regressing from an agricultural to a
hunter-gatherer state of subsistence. Sather (1995) argues convincingly, however, that the Penan may indeed
reﬂect a secondary foraging adaptation, but that the
initial Austronesian subsistence economy would have
had to have been diverse, incorporating aspects of
maritime, cereal food production, cultivation of endemic
fruit trees and root crops, and foraging forays along
strand lines and hunting a diversity of medium-large
mammals associated with perhumid rain forests. Devolution is far oﬀ the conceptual mark in terms of the
adoption of secondary foraging as an adaptive subsistence regime (Brosius, 1991).
‘‘Broad spectrum’’ is a phrase commonly used to describe the diet of prehistoric people inhabiting rain forests with an eclectic dietary repertoire that may or may
not include some form of systematic food production
(e.g., Hutterer, 1988). Broad spectrum implies a continuum of sorts between pure foraging subsistence on one
hand versus one with foraged foods supplemented by
systematic tending of plants grown alongside their homes
and in small systematically maintained swidden plots
(Harris, 1989). Food remains at prehistoric sites tend to
consist of fragmentary faunal remains representing a
diverse array of vertebrate and invertebrate species
common in rain forest and riverine/estuarine habitats
(Bailey et al., 1989; Gorman, 1971; Medway, 1958;
Medway, 1979). Although these remains are consistent
with a hunting-based economy, the evidence seems to be
diﬀerentially biased against the preservation of subsistence-related botanical remains (e.g., Hather, 1994).
Further, as Harris (1989) has emphasized, characterizing the presence of ÔagricultureÕ is not always so
clear-cut because the distinction between wild plant
foraging and the cultivation of plant foods is likely one
that diﬀered by degrees along a continuum. Broad
spectrum subsistence therefore might be inferred based
on analyses of faunal remains recovered even if farming
to one degree or another was practiced. There is a simple
explanation for this. During and after agricultureÕs
presence in the region, hunting and gathering continued
to be an important dietary component for many groups,
including those who were involved to some degree on
subsistence farming (e.g., Headland and Reid, 1989;
Junker, 1996; Sather, 1995). Others likely opted not to
participate in food production in the strict sense. Such
circumstances, it could be argued, are more commonplace in areas less conducive to growing agricultural
crops. In tropical Southeast Asia, therefore, it has been
diﬃcult to identify the foraging-farming transition,
much less characterize it as either a synchronized phenomenon or a dramatic, punctuated event.
The sites
There are three key Neolithic sites in the East Malaysian state of Sarawak in northern Borneo (Fig. 1). All
sites are situated in karst limestone terrain and primary
rain forest. All contain aspects of material culture and
mortuary ritual that are characteristic of the Neolithic
period in the Indo-Malaysian archipelago (Bellwood,
1992, 1997). Table 1 lists the most recent compendium of
uncalibrated 14 C dates for each siteÕs Holocene component. Fig. 2 charts their 2 SD range (2r), providing a
rough picture of site chronology.
Niah Cave. For many years, SarawakÕs prehistory
was based principally on the ﬁndings from Niah CaveÕs
West Mouth (Harrisson, 1972). The West Mouth is part
of an extensive 13 km2 limestone massif receiving capital
attention both for its sheer size and the extent of archaeological excavations conducted there over the past
50 years. It has produced one of the largest archaeological assemblages yet excavated in island Southeast
Asia with both late Pleistocene and Holocene cultural
contexts well represented (Barker et al., 2000, 2002, in
press; Bellwood, 1997; Harrisson, 1957, 1959a, 1972;
Krigbaum, 2001; Zuraina, 1982).
Recent analysis of all available good Holocene 14 C
dates from charcoal and coﬃn wood demonstrate a
4000+ year gap in the sequence between the late/termi-
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
Table 1
Uncalibrated Holocene
Lab/sampleb
14
C dates for Niah Cave (West Mouth)a , Gua Sireh, and Lubang Angin (Sarawak, East Malaysia)
Burial/provenience
Niah Cave (West Mouth)
GX-4836
N/A
GX-4917
N/A
GrN-7204C
75 (extended)
AA-27957
50 (extended)
GX-1428
159 (burnt)
GrN-7202
75 (extended)
GrN-1905
N/A
GrN-1907
60C (multiple)
GX-0721
60C (multiple)
GX-4837
N/A
Gua Sireh
M-1029
ANU-7046
CAMS-721
Pit c/10 (6’’)
G8N, layer 2
89A, layer 3
ANU-7047
CAMS-725
G8N, layer 3
F8S, 20–25 cm
ANU-7049
A-283
ANU-7045 (B)
G8N, layer 4/6 [20–25 (2)]
G8N, layer 7/8 [20–25 (I)]
ANU-7050
G8N, layer 9 (top) [35–40]
Lubang Angin
ANU-7044
295
LA3 [N] 40 cm
CAMS-727
LA-3
CAMS-728
LA-6-1
CAMS-729
LA-6-2
Sample material
d13 Cc
14
Charcoal
Charcoal
Burial matting
Charcoal
‘‘Rotted’’ wood
Coﬃn wood
Charcoal
Coﬃn wood
Coﬃn wood
Charcoal
N/A
N/A
N/A
)27.0
N/A
N/A
N/A
N/A
N/A
N/A
9885 175
8565 240
3495 100
3285 50
3175 105
3080 40
2700 70
2695 65
2620 220
1635 115
1
2,
4
3
5
4
7,
7,
6
2,
Charcoal
Charcoal
Rice husk in
sherd
Charcoal
Rice grain in
sherd
Charcoal
Charcoal
Freshwater
shell, Brotia sp.
Freshwater
shell, Brotia sp.
N/A
)19.3 0.2
N/A
425 150
990 130
1480 260
9
10, 11
10, 12
)18.8 0.2
N/A
3300 190
3850 260
10, 11
10, 12
N/A
N/A
)12.3 0.4
3990 230
4480 100
5290 80
10, 11
13
10, 11
)11.6 0.4
5610 80
10, 11
)10.4 0.4
2400 135d
10, 11
N/A
1650 90
10
N/A
1960 90
10
N/A
2200 120
10
Marine shell,
Batissa sp.
Human bone
‘‘collagen’’
Human bone
‘‘collagen’’
Human bone
‘‘apatite’’
C Age B.P.
Refse
3
8
8
3
a
Only ‘‘good’’ charcoal dates included for Niah Cave (West Mouth), not including dates in Barker et al. (2002, in press).
Lab codes: GX, Geochron; GrN, Groningen (nb. ‘‘C’’ suﬃx indicates correction to original date); AA, University of Arizona
AMS; M, University of Michigan; ANU, Australian National University; CAMS, Lawrence Livermore AMS Facility; A, University of
Arizona. ANU 14 C dates have been updated based on ANU Radiocarbon Dating Laboratory corrections, via personal communication
with Peter Bellwood (ANU). [ ], information on ANU 14 C reports. ANU d13 C values reported where possible courtesy Peter Bellwood.
c 13
d C values determined for ‘‘AA’’ AMS dates.
d
Original calculated date ¼ 2850 100 years BP. Date listed is corrected for oceanic reservoir eﬀect following Gillespie and Polach
(1979).
e
References: 1, Zuraina (1982); 2, unpublished (courtesy Zuraina Majid); 3, Krigbaum (2001), 4, Harrisson (1975), 5, Harrisson
(1968), 6, Harrisson (1967), 7, Vogel and Waterbolk (1963), 8, Harrisson (1959b), 9, Crane and Griﬀen (1962), 10, Ipoi and Bellwood
(1991); 11, Ipoi (1993), 12, Bellwood et al. (1992); 13, Damon et al. (1963).
b
nal Pleistocene and mid-Holocene (Fig. 2). Although
sample size of charcoal is small (Table 1), the lack of 14 C
dates and their error range overlapping the period 8000–
4000 years BP suggests a hiatus in human use of the cave
that may be both environmental and cultural in nature
(Krigbaum, 2001). If this gap is real, it may be indicative
of a natural transition/replacement in human populations from pre-Austronesian to Austronesian. Addi-
tionally, mid-Holocene ecological constraints could have
made the site less conducive to habitation. By Neolithic
times, the site was used primarily as a place for mortuary
ritual and a respite rather than a habitation site, as was
its function during the late Pleistocene/early Holocene
(Bellwood, 1997; Krigbaum, 2001).
The Neolithic component at Niah Cave (after ca.
3500 years BP) is fairly well dated. It is characterized by
296
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
Fig. 2. Uncalibrated Holocene 14 C dates for Niah Cave (West Mouth), Gua Sireh, and Lobang Angin. Dates are plotted with 2 SD
range (2r). Only charcoal dates for Niah Cave (West Mouth) are plotted (see Table 1 for details).
a number of elaborate primary and secondary burials
associated with pottery and polished stone tools. The
Neolithic human burial series, as classiﬁed by Barbara
Harrisson (1967), includes Extended primary inhumations usually in coﬃns and/or wrapping, Burnt secondary burials (usually in earthenware jars), and Cremation
secondary burials (partially to fully calcined). Fragmentary faunal remains show evidence of a diverse
hunting regime, dominated by wild boar, porcupine, and
a variety of primates (Medway, 1958, 1979). However,
distinguishing subsistence remains between pre-Neolithic and Neolithic contexts is near impossible because
of extreme mixing of subsurface levels due to concentrated mortuary activity.
Gua Sireh. Gua Sireh is an important archaeological
site in eastern Sarawak. Since the 1950s, this site has
received steadfast attention by aﬃliates at the Sarawak
Museum, however not until Ipoi Datan and Peter Bellwood conducted systematic ﬁeld excavations was a
proper publication prepared (Ipoi, 1993; Ipoi and Bellwood, 1991). A number of 14 C dates have been run on
organic materials from this site (Table 1). Of note is an
AMS date of 3850 260 14 C years BP (ca. 4200 years
BP) obtained on rice husk inclusions (as temper) in
pottery that represent the earliest date for the presence
of rice in island Southeast Asia (Bellwood et al., 1992).
The presence of rice at Gua Sireh has also been conﬁrmed in sediments (Beavitt et al., 1996). Several extended human burials were recovered which date to the
Neolithic/Early Metal Period. An open question at
present is whether Gua SirehÕs Neolithic assemblage
reﬂects the early presence of Austronesian speaking
peoples, Austroasiatic expansion from mainland
Southeast Asia, or both. As evident in Fig. 2 with the
range of Gua Sireh dates, a Neolithic phase that slightly
precedes that at Niah Cave is plausible.
Lubang Angin. Another small site excavated recently
(Ipoi, 1993; Ipoi and Bellwood, 1991) is Lubang Angin
located in the interior of Sarawak within Mulu National
Park, not far from the present Brunei border. Here
terrain is more rugged and mountainous and habitat
more varied then at the lowland sites of Niah Cave or
Gua Sireh. Social links with Niah Cave are suggested,
based on ﬁndings of material culture and burial conﬁguration. Contact with the coast is indicated by the
presence of marine shell. Based on bone and shell 14 C
dates, Lubang Angin reﬂects human presence towards
the later stages of the Neolithic/Early Metal Period
(Table 1, Fig. 2).
Isotopic variations in dietary resources and natural
environments
Human teeth recovered from these Neolithic sites
permit paleodietary analysis to be performed, here focusing chieﬂy on the stable isotopes of carbon and oxygen within the tooth enamel. Isotopes of a given
element diﬀer in the number of neutrons present in their
nuclei, and this inﬂuences their atomic weight. There are
three isotopes of carbon, one unstable and radioactive
(14 C), and thus subject to change, and two stable (13 C
and 12 C), whose masses are unchanged over time. Differences in 13 C/12 C ratios of dietary resources permit
stable isotope analysis of bone and tooth tissues in
paleodietary studies. There are two dominant isotopes
of oxygen (18 O and 16 O), both stable, whose isotopic
ratio 18 O/16 O may be used as a proxy for temperaturedependent biological systems.
The abundance of stable isotopes within a given
sample—its isotopic ratio—is compared to the ratio of
a known standard. The ﬁnal calculated ratio—the delta
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
C-13 value (d13 C) is expressed in parts per thousand or
per mil (‰) diﬀerence from a standard. In delta notation, the equation used to express the isotope ratios of a
sample A relative to a standard is as follows:
dAð‰Þ ¼ ðRsample Rsample =Rstd Þ 1000
or
¼ ðRsample =Rstd 1Þ 1000;
where R is 13 C/12 C or 18 O/16 O, and the standards are the
Peedee Formation belemnite (PDB) and standard mean
ocean water (SMOW), respectively.
Diﬀerences in mass inﬂuence the chemical reaction
rate of each isotope: lighter isotopes (i.e., those with
fewer neutrons) are more mobile and react faster than
heavier ones. Complex physiological and environmental
factors either select for or discriminate against heavier
isotopes over lighter ones, and result in systematic isotopic variations in nature (Hoefs, 1997). This fundamental phenomenon, referred to as fractionation, causes
subtle, but measurable diﬀerences in isotope abundance
in biogenic materials that can be related to biological
processes such as photosynthesis, food metabolism, and
temperature (Ambrose, 1993; Koch et al., 1994; Pate,
1994; Schoeninger, 1995; Schoeninger and Moore, 1992;
Schwarcz, 2000). Data are obtained using mass spectrometry, and the overall standard deviation of analyses
is less than 0.05‰ for carbon and 0.2‰ for oxygen.
Stable carbon isotopes can distinguish between terrestrial plants that follow diﬀerent photosynthetic
pathways. The two principal pathways involve C3 and
C4 plants. Most terrestrial plants, including trees, herbs,
shrubs, temperate and high altitude grasses, follow the
C3 pathway. Their d13 C values average )27‰ and show
a broad range, between ca. )20‰ to )35‰ (OÕLeary,
297
1981; OÕLeary, 1988). C4 plants include arid-adapted
grasses and sedges. They average )12.5‰, and have a
narrower range between ca. )7‰ to )6‰. Signiﬁcantly,
the values of these two groups of plants do not overlap.
In this study, it is the broad isotopic range of C3 plants
that is of interest as C4 cultigens were likely an insigniﬁcant component of the diet in prehistoric Borneo.
Fig. 3 outlines the canopy eﬀect phenomenon and its
inﬂuence on d13 C values in closed vs. open forest conditions. Average values for C3 plants, occur at the top of
the canopy, where modern CO2 is ca. )7.8‰. However,
in closed canopy forests, more negative values occur in
the understory because of the contribution of biogenic
CO2 from C3 plant root respiration and soil organic
matter decomposition. Decreasing d13 C values in leaves
and air have been documented along a vertical gradient
from canopy top to forest ﬂoor in every ecosystem
studied (e.g., Ambrose, 1993; Heaton, 1999; Krigbaum,
2001; Medina and Minchin, 1980; van der Merwe and
Medina, 1989, 1991; Vogel, 1978). Within the forest,
CO2 is most negative near the forest ﬂoor, with d13 C
values as low as )14‰ in deep tropical forests (van der
Merwe and Medina, 1989, 1991). Contributing to this is
soil-respired CO2 , which is considerably depleted in 13 C
(compared to air), with more negative d13 C values
ranging from )25‰ to )28‰ (Jackson et al., 1993;
Vogel, 1978). The decreasing leaf d13 C values of the
canopy eﬀect are likely a result of two interdependent
factors: (1) decreased light levels, or irradiance, due to
closed canopy conditions (e.g., Broadmeadow and
Griﬃths, 1993; Ehleringer et al., 1986); and (2) recycled
CO2 becoming incorporated within the plants of the
understory (e.g., Sternberg et al., 1989; Vogel, 1978).
These same isotopic trends have been documented in
Fig. 3. Generalized model of d13 C variation in closed and open conditions. Low irradiance and recycled CO2 result in lower d13 C
values in air, soil, and vegetation in contrast to more open areas where there is high irradiance and no recycling of CO2 . Open areas
tend to have C3 plants that are near the average for C3 vegetation (ca. )27‰). In closed areas, understory vegetation is signiﬁcantly
depleted in 13 C and C3 vegetation has more negative values ( 6 )30‰). Adapted from Quade et al. (1995) and Jackson et al. (1993).
298
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
endemic plant foods and cultigens collected under
varying degrees of forest closure in Sarawak (Krigbaum,
2001).
Freshwater aquatic systems tend to follow a C3 -like
pathway, however, carbon in dissolved CO2 can come
from any number of sources (detritus of carbonate
rocks, mineral springs, atmospheric CO2 , recycled organic matter) and d13 C values may vary widely as a result of these complex factors (Peterson and Fry, 1987).
Marine phytoplankton also follow the C3 pathway, their
source carbon being dissolved CO2 in seawater, a
product of bicarbonate. In general, the d13 C of marine
plants reﬂects the equilibrium oﬀset observed between
atmospheric CO2 and marine bicarbonate (ca. )7‰).
Whereas terrestrial plants average )27‰, marine
plankton have d13 C values that average between )19‰
and )21‰ (Ambrose, 1993).
A plantÕs isotopic composition is maintained in the
food chain by a series of fractionation events—positive
shifts, or oﬀsets in d13 C value—especially between plants
and their primary consumers. The old adage ‘‘you are
what you eat’’ is accurate with respect to carbon, and
depending upon what tissue is analyzed, one adds the
appropriate oﬀset to interpret the results. For example,
the oﬀset of tooth enamel is between 9.5‰ for carnivores
to 14‰ for ruminant herbivores (Ambrose and Norr,
1993; Cerling and Harris, 1999; Koch et al., 1994;
Krueger and Sullivan, 1984). Based on these ﬁgures,
tooth enamel values would be expected to fall anywhere
between )17‰ and )13‰ for a pure C3 vegetarian diet.
This variation in spacing has often been interpreted as a
trophic level eﬀect (Krueger and Sullivan, 1984; LeeThorp et al., 1989). However, if the large oﬀset for
herbivores is related to isotopic eﬀects of methanogenesis by symbiotic digestive bacteria in large herbivores
(Ambrose et al., 1997; Schwarcz, 2000), then the 9.5‰
oﬀset may be more appropriate for humans.
Consumers in closed forest habitats similarly reﬂect
the canopy eﬀect in their biological tissues. Preliminary
isotopic analysis of the Niah Cave fauna (Krigbaum,
2001) demonstrates a consistent pattern of increasingly
negative d13 C values (ca. )18‰ to )14‰) among omnivorous browsers such as barking deer (Muntiacus
muntjak), mouse deer (Tragulus napu), the grazer banteng (Bos javanicus), and omnivorous bearded pig (Sus
barbatus). Although not as dramatically negative as the
consistent browser okapi (Okapia) from the Ituri Forest
with d13 C values from )22‰ to )20‰ reported by
Cerling and Harris (1999), the Niah Cave fauna both
taxonomically and isotopically do document a closed
canopy setting (Krigbaum, 2001).
A number of diverse studies demonstrate a similar
pattern. Schoeninger and colleagues (1997) examined
arboreal New World monkeys distinguishing preferred
habitat using stable carbon isotopes derived from hair
samples. Primate taxa (Alouatta and Cebus) with con-
sistently less negative d13 C values were adapted to drier,
deciduous forest, whereas, those taxa inhabiting perhumid forest (Ateles and Brachyteles) exhibited more
negative d13 C values, indicative of increased water stress
in drier habitats. Froment and Ambrose (1995) studied
diﬀerent human populations in Cameroon inhabiting
equatorial rain forest, but participating in diﬀerent
modes of subsistence from hunting and gathering to
food production. Sampling hair, d13 C values for interior
groups were from )28‰ to )23‰ with the huntergatherer groups not involved in agriculture consistently
more negative in isotopic value.
Materials and methods
Three adults were sampled from Lubang Angin, ﬁve
from Gua Sireh, and 28 Neolithic burials from Niah
Cave (West Mouth). Selected human tooth enamel
samples (M3s preferred) were cleaned of adhering debris
and dentine using a Dremel tool with a carbide bit and
inspected under a binocular microscope prior to grinding. Cleaned tooth enamel was oxidized in a 2% solution
of Clorox for about 16 h to remove humic acids and
organics; rinsed in distilled H2 O to normal pH and
pretreated with 0.1 M acetic acid for 16 h to remove any
diagenetic and adsorbed secondary carbonates, and
rinsed again to normal pH with distilled H2 O. Samples
were then lyophilized (freeze-dried) and converted to
CO2 by reaction with 100% phosphoric acid for 2 h at
90 °C. After passing the evolved CO2 through a silver
phosphate trap to remove contaminant sulphur (evolved
H2 S or SO2 ), the CO2 gas was collected by cryogenic
distillation. Stable isotope ratios for carbon and oxygen
derived from tooth enamel apatite (structural carbonate)
were then measured on a Finnigan MAT 251 mass
spectrometer at Yale UniversityÕs Stable Isotope Laboratory. Percent carbon yields were determined by regression coeﬃcients based on repeated trials of the NBS
19 carbonate standard.
Results and discussion
The human tooth enamel d13 C results for Neolithic
Niah Cave (West Mouth), Gua Sireh, and Lubang Angin are presented in Tables 2–4. Fig. 4 presents all individual data with d13 C values plotted along the x axis
and oxygen isotope values (d18 O) along the y axis. d18 O
values aid in the partitioning of the data. The Niah
Neolithic results are presented by burial type, sexes
pooled. Table 5 lists the descriptive statistics for d13 C
and d18 O (N, mean, standard deviation, range), and includes pre-Neolithic individuals (N ¼ 15), not presented
in this study (Krigbaum, submitted). Focusing on the
stable carbon isotope values, collectively these data
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
299
Table 2
d13 C and d18 O results (tooth enamel apatite) for Neolithic human burials from Niah Cave (West Mouth), by burial ‘‘type’’
Burial No.a
Tooth
Ageb
Sex
Burial typec
d13 C (‰ PDB)
d18 O (‰ SMOW)
% C Yieldd
3
10
36
40
41
45
48
50
57
60A
60C
68
75
102
104
110
115
123
126
128
133
164
49
96
30
53
103B
129
LM3
LM3
LM3
LM3
LM3
LM3
LM3
RM3
RM3
RM3
LM3
LM3
LM3
LM3
LM3
?LM2
RM3
RM3
LM3
LM3
RM3
LM3
LM3
RM3
LM2
RM3
RM3
RM3
M.A.
M.A.
M.A.
Y.A.
A
M.A.
A
M.A.
M.A.
M.A.
M.A.
M.A.
Y.A.
Y.A.
O.C.
M.A.
Y.A.
Y.A.
M.A.
Y.A.
Y.A.
A
A
Y.A.
A
A
M.A.
Y.A.
M
F
F
M
?
F
?
F
M
M
F
F
F
F
?F
F
M
F
M
M
F
?
?
F
?
?M
?M
F
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Multiple
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Extended
Cremation
Cremation
Burnt
Burnt
Burnt
Burnt
)11.9
)13.0
)12.7
)13.8
)13.6
)12.8
)13.6
)13.7
)13.7
)13.5
)12.6
)14.7
)12.3
)13.1
)13.5
)12.2
)11.3
)14.7
)13.3
)14.0
)13.3
)13.5
)12.0
)12.7
)13.7
)13.3
)14.8
)13.0
23.9
23.7
24.3
22.5
24.1
24.2
22.9
23.4
24.0
24.3
23.3
23.8
23.7
23.9
23.5
23.5
22.9
23.8
23.1
24.8
23.7
23.7
24.6
24.8
24.6
24.2
23.2
23.6
0.76
0.63
0.71
0.65
0.69
0.62
0.65
0.59
0.67
0.62
0.62
0.24*
0.61
0.64
0.56
0.68
0.61
0.38*
0.59
0.45
0.59
0.67
0.62
0.57
0.69
0.63
0.55
0.57
a
Burial Nos. assigned by excavators (Harrisson, 1967).
Age categories as follows: ‘‘O.C.’’, older child (13–18); ‘‘Y.A.’’, young adult (18–35); ‘‘M.A.’’, middle adult (35–55); ‘‘A’’, adult.
c
Burial ‘‘type’’ as assigned by excavators (Harrisson, 1967).
d
Results producing low % C yields are indicated with an asterisk, and their d13 C and d18 O values are italicized.
b
Table 3
Gua Sireh d13 C and d18 O results (tooth enamel apatite) for Neolithic/Early Metal (?) human burials
Tooth
Age
Sex
Burial type
d13 C (‰ PDB)
d18 O (‰ SMOW)
% C Yield
M3
M3
M3
M3
M3
A
A
A
A
A
?
?
?
?
?
?Extended
?Extended
?Extended
?Extended
?Extended
)13.3
)13.0
)11.9
)12.5
)13.3
22.6
22.6
23.6
23.6
25.1
0.61
0.62
0.62
0.64
0.60
Table 4
Lubang Angin d13 C and d18 O results (tooth enamel apatite) for Neolithic/Early Metal (?) human burials
Tooth
Age
Sex
Burial type
d13 C (‰ PDB)
d18 O (‰ SMOW)
% C Yield
M3
M3
M3
A
A
A
?
?
?
Extended
Extended
Extended
)14.3
)14.6
)14.2
24.2
23.6
23.5
0.66
0.59
0.66
300
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
Fig. 4. d18 OSMOW and values d13 CPDB values (tooth enamel apatite) for Neolithic Niah Cave (West Mouth), Gua Sireh, and Lubang
Angin.
Table 5
Descriptive statistics for human d13 C and d18 O results (tooth enamel) by site including pre-Neolithic Niah Cave (West Mouth) for
comparison (see Fig. 5)
Pre-Neolithic
d13 C (‰ PDB)
N
Mean
SD
Range
d18 O (‰ SMOW)
N
Mean
SD
Range
Neolithic
Niah Cave
Niah Cave
Lubang Angin
Gua Sireh
15
)14.4
0.85
)15.7 to )12.2
28
)13.2
0.84
)14.8 to )11.3
3
)14.4
0.19
)14.6 to )14.2
5
)12.8
0.60
)13.3 to )11.9
15
24.2
1.11
21.9–26.2
28
23.8
0.58
22.5–24.8
show a diet dependent on C3 foodstuﬀs. Lubang Angin
individuals show an average of )14.4‰, Gua Sireh individuals have less negative d13 C values, averaging
)12.8‰, and Niah Neolithic burials average )13.2‰.
Fig. 5 plots the tooth enamel isotopic data by mean
and standard deviation, based on the summary data
presented in Table 5. This permits more clear temporal
distinction between pre-Neolithic and Neolithic d13 C
values at Niah Cave, and demonstrates how the Lubang
Angin individuals clearly cluster with the mean d13 C
values characteristic of the pre-Neolithic Niah Cave
sample. Gua Sireh individuals, in contrast, cluster with
the less negative Neolithic Niah Cave sample. StudentÕs t
test applied to these results are statistically signiﬁcant at
the .01 level—between sites for the Neolithic remains,
and within Niah for the pre-Neolithic vs. Neolithic remains sampled.
3
23.8
0.35
23.5–24.2
5
23.5
1.01
22.6–25.1
Several factors might account for these shifts towards
less negative d13 C values. A shift might occur with increased consumption of estuarine/maritime food resources (e.g., Chisholm et al., 1982). Although this seems
unlikely based on current knowledge of the fauna from
Niah Cave (bearded pig, porcupines, orang utans, and
monkeys), there is no doubt that invertebrates obtained
from coastal mangrove habitats (and riverine freshwater
habitats, for that matter) comprised part of the Neolithic diet of individuals recovered from Niah Cave.
Further, the study by Rodelli and colleagues (1984)
underscores the fact that estuarine foodstuﬀs have terrestrial d13 C values with minimal mixing of marine
carbon.
Another potential explanation is the adoption of C4
cultigens into the diet—probably not as a staple but as
an important supplement. Two likely candidates are
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
301
Fig. 5. Mean and SDs for d18 OSMOW and d13 CPDB values (tooth enamel apatite) for pre-Neolithic Niah Cave, Neolithic Niah Cave
(West Mouth), Gua Sireh, and Lubang Angin (see Table 5).
JobÕs tears (Coix lachryma-jobi) and foxtail millet (Setaria italica). For several diﬀerent reasons, mostly related to plant biogeography and climate, it is unlikely
these subtropical C4 cereal grains factored signiﬁcantly
into the diet of Neolithic people in perhumid Borneo
(Arora, 1977; Bellwood, 1997; Burkill, 1966). A more
plausible explanation for the increase in d13 C values is
that of increased reliance on plant foods grown in more
open conditions.
A continuum of sorts can be postulated between
those individuals that can be characterized by closed
forest foraging (more negative d13 C values) and those
characterized by open forest horticulture (less negative
d13 C values). The range of d13 C variation by burial type
at Niah suggests a number of diﬀerent subsistence patterns are represented in the Niah Neolithic sequence
(Krigbaum, submitted). Niah Cave may reﬂect a central
hub for mid-late Holocene Austronesian groups, but the
people that buried their dead at Niah Cave during the
Neolithic likely lived elsewhere, and were involved in
food production/collection systems to one degree or
another. The positive trend in d13 C values observed at
Gua Sireh also seems to reﬂect food production, but the
extent to which Gua Sireh is culturally related to Neolithic Niah Cave remains an open question. The earlier
Neolithic dates at Gua Sireh, and the unambiguous
presence of rice at that site, suggests potential Austroasiatic contact with mainland Southeast Asia (Beavitt et
al., 1996; Bellwood, 1997).
Aside from potential cultural aﬃliations, however,
human groups were literally making their mark on the
landscape during the Holocene (Maloney, 1998). Inferred subsistence regimes in this study likely involved
modiﬁcation of the landscape or use of natural clearings
to foster growth of certain food plant species. Paleobotanical studies in the region underscore the striking
impact prehistoric human groups had on the landscape
(e.g., Maloney, 1980; Stuijts, 1993).
Individuals at Lubang Angin have more negative
isotopic values more in line with closed forest foraging,
which may well reﬂect their adaptation to a secondary
foraging subsistence strategy more akin to pre-cultigen
broad spectrum subsistence inferred for the pre-Neolithic Niah Cave sample. In general, interior Sarawak is
an area where various Penan groups and their predecessors followed a nomadic existence dependent on wild
forest resources including hill sago (Eugeissona utilis)
and a variety of hunted game, mainly bearded pig (Sus
barbatus) (Brosius, 1991). Estuarine food resources were
not accessible and trade with neighboring agriculturalists likely occurred, but probably did not include subsistence items in return for forest resources (Brosius,
1991; Sather, 1995).
Conclusions
Broad spectrum subsistence implies a generalized
hunting, gathering, and ﬁshing-based resource sphere
where any number of foods may be eaten including wild
root crops, vegetables, nuts, fruits, honey, and harvested/hunted invertebrates (snails, shellﬁsh, insects,
etc.) and vertebrates (ﬁsh, reptiles, mammals). In tropical Southeast Asia, broad spectrum subsistence likely
characterized many hunter-gatherer groups and continued up to and after the origins of agriculture in the region (Bellwood, 1997; Sather, 1995). Certainly there are
still hunter-gatherer groups in Southeast Asia, isolated
from neighboring agricultural groups, who conform
more or less to this pattern of subsistence (Brosius, 1991;
Dentan, 1991; Eder, 1988; Endicott, 1984; Headland,
1987; Sellato, 1994). However, the bias everpresent in
302
J. Krigbaum / Journal of Anthropological Archaeology 22 (2003) 292–304
the archaeological record in lowland tropical contexts
needs to be repeatedly checked with new analytical
methods and questions. Stable isotopic data presented
here oﬀers one fresh perspective with which to infer new
patterns of prehistoric human subsistence patterns.
Early food production in the Neolithic of Borneo
likely involved endemic plants and fruits and potentially
non-native items such as rice (Oryza sativa). The early
Neolithic settlers in Borneo clearly had an eclectic subsistence, one that can be generalized as broad spectrum
based on the ecological context of the site and the faunal
remains recovered in the archaeological record. However,
isotopic analysis using stable isotopes from tooth enamel
demonstrate greater heterogeneity of diet that is signiﬁcant with respect to inferring diet and constructing models
for prehistoric subsistence and settlement. Neolithic
groups were faced with new challenges which may well
have involved adaptations towards secondary foraging
and/or systematic food production and collection. These
trends in diet likely reﬂect patterns that mirror larger,
more fundamental aspects of subsistence, settlement, and
mobility. Interpreting these data along a continuum between closed forest foraging and open forest horticulture
may help us better understand the complexities of this
record.
Acknowledgments
I thank the Sarawak Museum ﬁrst and foremost,
particularly Ipoi Datan, Sanib Said, and Edmund Kurui, for their interest in prehistory and permitting me
access to the Niah Cave collection. Further appreciation
goes to Sheilagh and Richard Brooks and Bernardo
Arriaza (Univ. Nevada, Las Vegas) for their generous
hospitality while examining Niah Cave remains in their
care. A number of colleagues and reviewers have contributed to the content of this paper, most importantly I
would like to acknowledge John Kingston, Terry Harrison, Stanley Ambrose, and Jessica Manser. Funding
was provided by pre-dissertation grants from WennerGren and NSF. A preliminary version of this paper was
presented at the 66th Annual Meeting of the Society for
American Archaeology (April 2001) in the sponsored
symposium ‘‘Pioneer in Paleodiet and the Radiocarbon
Dating of Bone: Papers in Honor of Hal Krueger’’
organized by the author and Stanley Ambrose.
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