Stable isotope evidence for dietary and cultural change over the Holocene at the Sabana de Bogotá region, Northern South America

Abstract

The Sabana de Bogotá in the northern Andes is an interesting region to investigate temporal patterns of dietary variation because it counts with a vast archaeological and osteological record for the last 10,000 years. In this paper stable isotope data of human archaeological bone collagen and apatite were used to study the evolution of diet and major subsistence transformations taking place during the Holocene (~9000- 600 cal BP). Paleoenvironmental reconstructions and the isotopic ecology of the Sabana de Bogotá were used as an interpretative baseline. Stable isotope measurements (δ13Ccol, δ13Cap, δ15N and Δ13Ccol-ap) representing hunter-gatherers, horticulturalists and agriculturalists (N=134 individuals) were analyzed using bivariate, regressional and discriminant statistical techniques. Results show that early Holocene hunter-gatherers (9000-7000 cal BP) consumed mostly C3 vegetal resources locally available. In contrast, animal protein was less important. Middle Holocene hunter-gatherers (6000-4500 cal BP) continued with the food-foraging pattern observed in the earlier counterparts and presented a slight increase in C3 animal protein intake. During the initial late Holocene ca. 4000 cal BP important shifts in subsistence strategies occurred when populations presented a trend towards mixed C3/C4 diets and by ca. 3500 cal BP there is a clear signal of C4 crops (i.e. maize) consumption concomitant with the introduction of ceramic technology. During the final late Holocene (last 2000 cal years BP) intensive agriculture was adopted and humans presented relatively diverse diets integrated by C4 and C3 crops, C3 - C4 feeding animals and freshwater resources. Such dietary change coincides with an increase in sociopolitical complexity, population size and a general decline in health.

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ORIGINAL PAPER
Stable isotope evidence for dietary and cultural change
over the Holocene at the Sabana de Bogotá region, Northern
South America
Miguel Delgado
1,2
Received: 9 May 2016 /Accepted: 29 September 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract The Sabana de Bogotá in the northern Andes is an
interesting region to investigate temporal patterns of dietary
variation because it counts with a vast archeological and oste-
ological record for the last 10,000 years. In this paper, stable
isotope data of human archeological bone collagen and apatite
were used to study the evolution of diet and major subsistence
transformations taking place during the Holocene (∼9000–
600 cal BP). Paleoenvironmental reconstructions and the iso-
topic ecology of the Sabana de Bogotá were used as an inter-
pretative baseline. Stable isotope measurements (δ
13
C
col
,
δ
13
C
ap
,δ
15
N, and Δ
13
C
col-ap
) representing hunter-gatherers,
horticulturalists, and agriculturalists (N= 134 individuals)
were analyzed by using bivariate, regressional, and discrimi-
nant statistical techniques. Results show that early Holocene
hunter-gatherers (9000–7000 cal BP) consumed mostly C
3
vegetal resources locally available. In contrast, animal protein
was less important. Middle Holocene hunter-gatherers (6000–
4500 cal BP) continued with the food foraging pattern ob-
served in the earlier counterparts and presented a slight in-
crease in C
3
animal protein intake. During the initial late
Holocene ca. 4000 cal BP, important shifts in subsistence
strategiesoccurred when populations presented atrend toward
mixed C
3
/C
4
diets, and by ca. 3500 cal BP, there is a clear
signal of C
4
crops (i.e., maize) consumption concomitant with
the introduction of ceramic technology. During the final late
Holocene (last 2000 cal years BP), intensive agriculture was
adopted and humans presented relatively diverse diets inte-
grated by C
4
and C
3
crops, C
3
-C
4
feeding animals, and fresh-
water resources. Such dietary change coincides with an in-
crease in sociopolitical complexity, population size, and a
general decline in health.
Keywords Stable isotopes .Cultural and dietary change .
Northern Andes .Holocene
Introduction
The Sabana de Bogotá (SB) in the northern Andes is a region
with substantial evidence of major subsistence shifts taking
place throughout the Holocene. Traditional conceptions indi-
cated that late Pleistocene/early Holocene hunter-gatherers
were specialized groups which relied heavily on large-sized
and medium-sized mammals and used a homogeneous and
specialized lithic industry named Abriense (Correal and van
der Hammen 1977;Correal1986,1990a;Hurtetal.1977;van
der Hammen et al. 1990). Despite the fact that reliable evi-
dence of extinct mammals like proboscidean gomphotheres,
xenarthrans, and American horses has been recovered (e.g.,
Tibitó), more recent interpretations suggest that generalist for-
agers with broad spectrum economies inhabited the region
during the late Pleistocene, developing throughout the early
Holocene diverse subsistence strategies with a strong focus in
plants and to a lesser extent in small/medium-sized mammals
(e.g., deer, guinea pig among others) (Aceituno et al. 2013;
Aceituno and Loaiza 2015; Borrero 2015; Cárdenas 2002;
Delgado et al. 2015a,b; Delgado 2015). Reassessments of
the radiocarbon chronology along with recent
Electronic supplementary material The online version of this article
(doi:10.1007/s12520-016-0403-3) contains supplementary material,
which is available to authorized users.
*Miguel Delgado
medelgado@fcnym.unlp.edu.ar
1
División Antropología, Facultad de Ciencias Naturales y Museo,
Universidad Nacional de La Plata, Paseo del Bosque s/n.
(B1900FWA), La Plata, República Argentina
2
Consejo Nacional de Investigaciones Científicas y Técnicas
(CONICET), Buenos Aires, República Argentina
Archaeol Anthropol Sci
DOI 10.1007/s12520-016-0403-3

technofunctional and bioarchaeological analyses suggest that
several groups relying on C
3
resources and with distinct lithic
traditions persisted and coexisted over this time span
(Aceituno and Rojas 2015;Delgado2015; Delgado et al.
2015a,b; Nieuwenhuis 2002).
During the middle Holocene non-local forager populations
with different settlement patterns, mortuary practices and skel-
etal morphology arrived in the region (Ardila 1984; Correal
and Pinto 1983;Correal1990b;Delgado2012a,2015).
Additionally, the appearance of tools for vegetal processing
(anvils, scrapers, hammerstones, among others) ca. 5800 cal
BP highlights the increasing importance of C
3
plant consump-
tion (Ardila 1984;Correal1990b). Certain cultigens, such as
squash (Curcubita pepo), oca (Oxalis tuberosa), and
Dioscorea dated around 4500 cal BP are thought to have been
introduced during this period (Ardila 1984;Correal1990b;
Cárdenas 2002). Skeletal and isotopic evidence indicates the
presence of abrasive diets and oral pathologies related to
higher consumption of non-processed foods, as well as conti-
nuity in C
3
plant consumption and changes in C
3
protein
sources (Cárdenas 2002; Delgado 2015;Gómez2012). The
increase in temperature/dryness and decrease in rainfall be-
tween ca. 7000 and 4500 cal BP caused important ecological
changes (i.e., reduction of water tables, habitat fragmentation,
etc.), which promoted multiple changes in hunter-gatherer
populations such as demographic contraction, population ex-
tinction, and dispersals (Delgado 2012a,2015).
The initial late Holocene period is central for our under-
standing of the adoption of agriculture given that important
changes in subsistence, demography, and food processing
technology occurred along with strong phenotypic diversi-
fication (Ardila 1984; Botiva 1989; Correal and van der
Hammen 1977; Correal and Pinto 1983; Correal 1990b;
Delgado 2012a,b,2015; Rodríguez and Colantonio 2015).
The isotopic evidence reveals diverse dietary patterns (C
3
,
C
3
/C
4
,andC
4
), which likely suggest that a change toward a
food production system likely began during that time
(Cárdenas 2002; Delgado 2015;vanderHammenetal.
1990). This is supported by the extensive archaeobotanical
evidence recovered from Aguazuque and Zipacón (ca.
4000/3500 cal BP), which reveals that local populations
were already consuming several C
3
and C
4
domesticated
plants by that time period (Correal and Pinto 1983;
Correal 1990b). Analyses of multiple bioarchaeological in-
dicators suggest a reduction in food consistence, an increase
in carbohydrates and silica-rich plant consumption, a higher
biological stress, population contacts/conflicts, and an in-
crease in population size (Delgado 2012a,2015;Gómez
2012;Rodríguez2006). The zooarchaeological and isotopic
record suggests a slight increase in animal protein consump-
tion and a diversification of animal resources (Correal and
Pinto 1983;Correal1990b;Cárdenas2002;Delgado2015).
During the final late Holocene, the archeological evidence
suggests that the most remarkable dietary change occurred
after 2000 cal BP, when people consumed considerably more
tropical plants (primarily, but not exclusively, maize) and an-
imal protein. For the last 1100 cal BP, during a period named
Muisca, divided into early (1000–700 cal BP) and late (700–
400 cal BP), the archaeobotanical and isotopic record, along
with ethnohistorical accounts (restricted to the late period),
stresses the importance of several cultigens (e.g., highland
tubercles, tropical grains, fruits, and palms) and diverse C
3
-
C
4
animal protein sources, including those from freshwater
ecosystems (Delgado et al. 2014;Enciso1996;García2012;
Langebaek 1987; Morcote 1996; Parra 2001; Simón 1981
[1625]). The skeletal evidence further supports the dietary
change as revealed by the increase in both occlusal dental
wear and the presence of certain pathologies indicating a very
high consumption of highly processed carbohydrates, iron
deficiency, and physiological stress (Delgado 2015;
Martínez 2012;Rodríguez2006).
As noted above, the major subsistence and dietary transfor-
mations in the study region have been addressed by using
distinct archeological indicators. While stable isotopes, which
provide quantitative dietary information at the individual lev-
el, have been used in previous studies of the region, an anal-
ysis by using a broad chronological and comparative approach
has never been undertaken. Therefore, the aim of the present
study is to investigate the main dietary/subsistence changes
which occurred in Sabana de Bogotá throughout the
Holocene (ca. 9000 to 600 cal BP) by using stable isotopes
of the bone collagen and apatite derived from human
archeological samples.
Samples and techniques
Currently, stable isotope analysis is a well-established tech-
nique widely used for reconstructing diet in distinct spatial
and temporal contexts. While not shown to be specific for
the area of this study, a common range in δ
13
C for C
3
/C
4
plants consumed by humans is from −24 to −10 ‰
(−14 ‰), with each per mil more positive than −24 ‰
representing about 7 % maize (or other C
4
plant) in the overall
diet (Katzenberg 2008;Schoeninger2009; Tykot 2004). Bone
collagen and bone apatite have resorption rates estimated at
7–10 years or more, so that isotopic analyses of adult bones
provide the average diet for many years prior to death (Tykot
2006,2014). Bone collagen δ
13
C is metabolically enriched
about +5 ‰relative to diet. It is known that while bone col-
lagen is disproportionately produced from the protein portion
of the diet, bone apatite is produced from a mixture of dietary
protein, carbohydrates, and fats (lipids) (Price and Burton
2011; Tykot 2004). The diet-apatite spacing differs according
to the model used and varies according to the C
3
and C
4
Archaeol Anthropol Sci

components of the diet. Under a model of +12 ‰for C
3
/C
4
dietary components, the value for mono-isotopic diets is
7.0 ‰,forC
3
protein/C
4
total diet is >7.0 ‰,andforC
4
total
diet/C
3
protein is <7.0 ‰(Tykot et al. 2009). Stable carbon
isotope analysis of both bone collagenand apatite thus permits
quantitative estimates of several dietary components.
Estimating the percentage of C
4
plants in human diet is
straightforward for herbivores and human agriculturalists, if
seafood was not available and animals were not consuming
wild C
4
grasses, by simple interpolation between the end-
points of bone apatite for a pure C
3
-based diet vs. a pure
C
4
-based diet (Kellner and Schoeninger 2007). Nitrogen iso-
topes generally reflect trophic-level differences between
plants and herbivores, and especially in multilevel aquatic
systems, so that the combination of N and C (both collagen
and apatite) isotope values allows discrimination between
these resource groups.
The available regional dataset includes 134 stable iso-
tope measurements (δ
13
C
col
,δ
13
C
ap
,δ
15
N, and Δ
13
C
col-
ap
), which were compiled from published sources
(Aufderheide 1990; Correal 1990b;Cárdenas1993,1996,
2002; Delgado et al. 2014; Rodríguez and Cifuentes 2005;
Rodríguez 2011;vanderHammenetal.1990). Such data
represent adult/adolescent (male and female) individuals
recovered from several archeological sites distributed in
the SB region (Table 1,Fig.1). Supplementary Table 1de-
tails the isotope data and sample composition investigated
here. Five main chronological/economic groups were stud-
ied (see Table 1) taking into account contextual
archeological and chronological information. This includes
early (∼9000–7000 cal BP) and mid-Holocene (∼6000–
4500 cal BP) hunter-gatherers, initial late Holocene
horticulturalists (∼3800–2200 cal BP), and final late
Holocene agriculturalists from the early (∼1015–800 cal
BP) and late Muisca (∼700–690 cal BP) periods. Despite
the presence of some chronological overlapping between
the early and late Muisca samples investigated, especially
between the upper and lower temporal ranges, such division
may shed interesting information regarding dietary diversi-
ty during the Muisca period. Radiocarbon dates were cali-
brated (2σ) by using the IntCal13 curve on the CALIB pro-
gram v. 7.0.4 (Stuiver and Reimer 1993). General trends
were investigated through bivariate comparisons, plots of
temporal dispersion, and mean differences (p< 0.05). The
regression model proposed by Kellner and Schoeninger
(2007) was used to obtain information on diet, dietary ener-
gy, and protein sources. Plots of δ
13
C
col
against δ
13
C
ap
pro-
vide a model of three regression lines (C
3
,C
4
, and marine
diet protein) where the position on each line indicates the
energy source (C
3
,C
4
, or mixed). In addition, the multivar-
iate statistical approach proposed by Froehle et al. (2012),
which includes not only carbon isotopes from bone collagen
(of δ
13
C
col
) and apatite (of δ
13
C
ap
) but also from nitrogen
(δ
15
N
col
), was used to distinguish dietary groups more clear-
ly. In order to determine the optimal number of clusters in
the dataset, a k-means cluster analysis was performed. Once
the most realistic number of groups was determined, a dis-
criminant function analysis (DFA) was carried out in order
to obtain significant linear functions and to identify vari-
ables that explain the multivariate distribution of individual
points and centroids. The analyzed dataset meets the as-
sumptions of multivariate normality within groups and
equality of covariance matrices among groups. The statisti-
cal and graphical analyses were performed in Systat 13 for
windows, Statistica 7.0 Statsoft Inc., and the free R software
(R Core Team 2015).
Tabl e 1 Samples analyzed by chronology, archeological site, and number of measurements per isotope
Sample Chronology Site δ
15
N
col
/
δ
13
C
col
δ
13
C
ap
/
Δ
13
C
col-ap
Reference
Early/middle Holocene
(EMH)
9000–7000 cal BP Checua
Galindo
La Floresta
a
Potreroalto
Tequenda ma
16 11 Cárdenas (2002), Rodríguez (2011),
van der Hammen et al. (1990)
Middle Holocene (MH) 6000–4500 cal BP Aguazuque 16 7 Aufderheide (1990), Cárdenas (2002),
van der Hammen et al. (1990)
Initial late Holocene (ILH) 3800–2200 cal BP Aguazuque
Madrid Tequendama
9 2 Aufderheide (1990), Cárdenas (2002),
Rodríguez and Cifuentes (2005),
van der Hammen et al. (1990)
Final late Holocene early Muisca 1015–800 cal BP Las Delicias Tibanica 66 66 Cárdenas (1993), Delgado et al. (2014)
Final late Holocene late Muisca 700–690 cal BP Candelaria
Portalegre
27 27 Cárdenas (1996,2002)
Total 134 113
a
La Floresta site is located in the Department of Boyacá but belongs to the cultural region integrated by the departments of Cundinamarca and Boyacá
named Altiplano Cundiboyacense
Archaeol Anthropol Sci

Paleoenvironmental reconstruction and the regional
isotopic ecology
Holocene environmental evolution
Based on palynological, glaciomorphological, isotopic, and dia-
tom evidence, detailed reconstructions of the predominant envi-
ronmental conditions have been performed for the SB region for
the last 13,000 years (Fig. 2). At the El Abra stadial (ca. 12,900–
11,800/10,900 cal BP), the regional equivalent to the Younger
Dryas Chronozone, the climate was very cold, with inferred tem-
peraturesbetween4to6°Clowerthantodayaccordingtopollen
data (van der Hammen and Hooghiemstra 1995)or3°Clower
than today in accordance to δ
13
C data derived from soil organic
matter (SOM) samples (Boom et al. 2001; Mora and Pratt 2002).
Biome reconstructions revealed a dominance of the cool
grassland-shrub biome (Marchant et al. 2002). Around
11,500 cal BP, the climate ameliorated again, with a sudden rise
in the average annual temperature (van der Hammen 1992). The
biome reconstructions for the 10,800–9500 cal BP interval re-
vealed that there was a remarkable expansion of mesic biomes,
which indicates a warm and wet period (Marchant et al. 2002).
Between ca. 8300 cal BP and ca. 6800/5800 cal BP, the record
shows vegetation changes, fluctuations in precipitations and tem-
perature with a tendency to dry environments, and the subsequent
decrease of water tables (Fig. 2)(Gómezetal.2007; Vélez et al.
2006). Biome reconstructions suggest a marked increase of the
cool mixed forest biome (Marchant et al. 2002). Between 5800
and 3800 cal BP, the paleoenvironmental record suggests an in-
crease in temperature (±2 °C) and a decrease in precipitation,
which caused a particularly dry period. After the 2500 cal BP,
climatic conditions became similar to what we know today
(Fig. 2). Pollen and sediment records suggest a high degree of
precipitation (reflected by an increase of marshy herbaceous veg-
etation and open water) as well as intensive human occupation
shownby deforestation (Quercus inparticular).In addition, pollen
Fig. 1 TheSabanadeBogotá
region showing the location of
archeological sites with human
and faunal skeletal remains
investigated. Checua (1),
Tequenda ma (2), Potreroalto (3),
Galindo (4), Aguazuque (5),
Madrid (6), final late Holocene
Muisca settlements (Portalegre,
Las Delicias, Candelaria,
Tibanica) (7)
Archaeol Anthropol Sci

data suggest lowering of water tables and increasing disturbance
probably caused by erosion (presence of Amaranthaceae/
Chenopodiaceae,Borreria,andDodonaea), crop cultivation
(presence of Zea mays), and frequent fires (as shown by the high
amounts of charcoal in the sediments) (Gómez et al. 2007; Vélez
et al. 2006). Biome reconstructions revealed an increase in the
cool grassland-shrub biome (Marchant et al. 2002).
Establishing the menu: the regional isotopic ecology
Stable isotope data provide reliable quantitative information on
diet at the individual level but requires an interpretative context
with respect to the potential resources that may have been con-
sumed. Such context is termed isotopic ecology, and it is useful to
define the regional dietary spectrum. Regarding vegetal re-
sources, we can obtain some information from isotope-based
paleoenvironmental research on the Holocenic altitudinal expan-
sion of wild C
4
vegetation (Boom et al. 2001; Guillet et al. 1988;
Mora and Pratt 2002) and from previous human stable isotope
studies (Cárdenas 1993,1996,2002; Delgado et al. 2014).
According to paleoenvironmental studies, elevated δ
13
Cvalues
ranging from −9to−15 ‰within the Andean/sub-Andeanforests
and moorland vegetation belts are indicative of the presence of C
4
and CAM plants during different moments of the Holocene
(supplementary Table 2). For the early/mid-Holocene, some au-
thors hypothesized that the presence of mixed C
3
/C
4
vegetation
can be explained by the expansion of lowland C
4
grasses caused
by lower partial atmospheric CO
2
pressure (pCO
2
), reduced rain-
fall, and temperature fluctuations related to rapid climatic chang-
es, whereas human-induced deforestation and/or cultivation of C
4
crops (maize mainly) and environmental rearrangements could
explain the presence of C
4
vegetation in the late Holocene
(Boom et al. 2001; Guillet et al. 1988; Mora and Pratt 2002).
With regard to maize consumption, previous studies on Muisca
human skeletal remains (Cárdenas 1993,1996,2002;Delgado
et al. 2014) suggest that carbon values ranging from −12.8 to
−9.7 ‰likelycorrespondwithamaize-based diet. Isotopic data
derived from Native American skeletons from the colonial period
suggest that values averaging −9.7 ‰or higher are indicative of
diets based mostly on maize consumption (Cárdenas 2002;
Delgado 2007). Although the isotopic research on faunal material
is scarce, it has allowed us to make some inferences although
restricted to the late Holocene (Table 2; Delgado et al. 2014). As
expected, carbon isotopes of two deer samples (Odocoileus
virginianus) reflect a C
3
diet, which likely reveals intra-specific
differences. However, when compared to fossil and experimental
evidence (Emery et al. 2000;Kohnetal.2005), they seem to have
been enriched. Carbon enrichment is more evident in the guinea
pig and rabbit samples (Table 2), whose values resemble a C
3
/C
4
diet. Despite the fact that human influence may have been a factor,
especially for cavia given its probable domestication date
established at ca.3500–2600 cal BP (Correal and Pinto 1983;
Fig. 2 Climatic-vegetation evolution and biome reconstructions for the
Sabana de Bogotá region for the last 19,000
14
C years on the basis of
palynological, glaciomorphological, and diatom evidence (adapted from
Delgado 2012a). Pantano de Vargas pollen zone (Zone VG). The gray
bars shows the chronological position of the Guantiva interestadial, El
Abra stadial, and the mid-Holocene climatic optimum
Archaeol Anthropol Sci

Ijzereef 1978), similar values in rabbit and the detection of C
4
and
CAM plants in the study region during the late Holocene likely
indicate the consumption of C
4
wild grasses by these animals. The
high nitrogen value found in the rabbit sample is not in line with
theirfeeding habitsand local ecologyas they can only getnitrogen
from the plants they consume. Nitrogen data from carnivorous
speciessuchasdog(Canis familiaris)andmargay(Leopardus
wiedii) revealed their higher trophic position within the local ter-
restrial food web. Carbon values resembling a C
4
diet can be
explained by the omnivorous dietary profile of dog and/or human
influence and a wide geographic range and feeding behavior for
margay, which includes small/medium-sized mammals and birds
that inhabit both the tropical lowlands and Andean highlands.
Finally, data for a duck species (Dendrocygna auntumnalis)re-
veal a C
3
diet complemented with freshwater resourc es( e.g., mol-
lusks), which indicates highland open water habitats (Moreano
2011).
Results
Univariate and bivariate comparisons
In Tables 3,4,and5and Figs. 3and 4,themain
chronological/economic trends for the groups under study
are presented. By the early Holocene, the low δ
13
C
col
values
indicate a high dependence on C
3
plants. In addition, one
individual presented a mixed C
3
/C
4
diet (see Figs. 3a and
4a). Nitrogen isotope ratios (Figs. 3a, b and 4b) revealed two
subgroups with low and mean values, respectively, which
suggests the presence of distinct protein sources (C
3
plants
and several C
3
-feeding animals) at that time. During the mid-
dle Holocene, people continued consuming basically C
3
plants and there is also a certain increase in nitrogen, which
reflects higher consumption of C
3
-consuming animals and
likely freshwater resources. Early and mid-Holocene samples
did not present significant differences in their diets (Tables 4
and 5). The carbon isotope data for the initial late Holocene
show some changes regarding previous periods, since while
some individuals maintained a C
3
dietary profile, others pre-
sented either mixed C
3
/C
4
or C
4
diets. During this time, the
slight increase in nitrogen reveals changes in protein sources
and/or increase in protein consumption. This trend is rein-
forced by the ttest revealing further differences in carbon
(collagen) and nitrogen (Tables 4and 5) with other time pe-
riods. For the final late Holocene, there was a clear C
4
signal
indicating more reliance on tropical crops, primarily maize
along with other C
3
and C
4
plants. There is also a considerable
increase in nitrogen and apatite values (Figs. 3and 4b, c),
which indicates a period of higher consumption of C
3
-C
4
an-
imals and freshwater resources. Interestingly, some differ-
ences emerged when the early and late Muisca samples were
compared such as the higher protein consumption during the
late period (Figs. 3and 4and Tables 3,4,and5). Furthermore,
Tabl e 2 Stable isotope
measurements for faunal samples
from the Sabana de Bogotá region
(data from Delgado et al. 2014)
Lab code Species δ
13
C
col
δ
15
N
col
δ
13
C
ap
Δ
13
C
col-ap
C/N
USF 14628 Odocoileus virginianus −18.6 7.8 −12.1 6.6 3.2
USF 14629 Odocoileus virginianus −19.1 6.0 −10 9.1 3.4
USF 14633 Cavia porcellus −16.6 7.3 −9.7 6.9 3.4
USF 14634 Sylvilagus brasiliensis −17.0 9.6 −8.9 8.1 3.5
USF 14632 Leopardus wiedii −16.1 8.8 −11 5.1 3.3
USF 14630 Canis familiaris −16.9 9.4 −11.1 5.8 3.4
USF 14631 Dendrocygna autumnalis −24.1 7.9 −14.2 10.0 3.3
Tabl e 3 Stable isotope summary statistics for the chronological/economic groups analyzed from the Sabana de Bogotá
Sample δ
13
C
col
SD Range δ
13
C
ap
SD Range δ
15
N
col
SD Range Δ
13
C
col-ap
SD Range
EMH
a
−20.0 0.49 −20.6–−18.8 −14.0 1.75 −16.3–−11.75 7.84 1.42 5.6–10.0 6.1 1.71 4.1–8.3
MH
b
−19.7 0.52 −20.6–−18.3 −14.5 0.82 −15.5–−12.9 8.58 1.31 6.3–11.2 5.5 1.1 4.4–7.4
ILH
c
−15.2 3.9 −20.2–−10.4 −14.7 0.59 −15.1–−14.2 8.83 0.94 7.12–9.9 5.4 0.61 5.0–5.8
FLHEM
d
−11.8 1.32 −15.8–−8.4 −8.4 3.31 −16.3–−4.1 9.4 0.67 8.2–10.4 5.0 0.89 3.2–8.3
FLHLM
e
−11.7 1.22 −13.9–−9.3 −7.2 1.0 −8.9–−5.1 10.3 1.04 8.4–12.1 4.5 0.70 3.2–6.2
a
EMH: early/middle Holocene hunter-gatherers
b
MH: middle Holocene hunter-gatherers
c
ILH: initial late Holocene hunter-gatherers/horticulturalists
d
FLHEM: final late Holocene agriculturalists from the Early Muisca period
e
FLHLM: final late Holocene agriculturalists from the Late Muisca period
Archaeol Anthropol Sci

the diet-apatite spacing values (Fig. 4d) suggest diets integrat-
ed by C
3
carbohydrates and C
3
protein sources during the
early and middle Holocene, C
4
carbohydrates and C
3
protein
during the initial late Holocene, and C
4
carbohydrates and C
3
-
C
4
protein by the final late Holocene.
Regression analysis
Figure 5illustrates the results of Kellner and Schoeninger’s
(2007) model. Individuals varied substantially in their source
of dietary energy and dietary protein over time, with opposite
patterns during the final late Holocene and the early/mid-
Holocene. As indicated by the model, while most final late
Holocene individuals show a strong emphasis on C
4
dietary
energy sources, some late individuals fall near the C
4
line, albeit
their position is closer to mixed C
3
/C
4
dietary energy. At least
one individual presented exclusively a C
3
protein source. The
regression results are consistent with the bivariate comparisons
and the ttest since they revealed slight differences between the
early and late Muisca periods in carbon isotopes. Overall, the
data corresponding to the final late Holocene showed that 50–
70 % of dietary protein and dietary energy came from C
4
sources. Early and mid-Holocene hunter-gatherers fall along the C
3
protein line with no or few C
4
signal, except for one
individual showing mixed C
3
/C
4
protein sources. With the ex-
ception of the aforementioned outlier, about 80–100 % of their
dietary energy came from C
3
sources. In addition, isotope data
for the first 5000 years of the Holocene show homogeneous
dietary sources and relatively diverse energy sources. Although
the initial late Holocene sample is underrepresented, the two
samples analyzed here have similar values to those from the
early and mid-Holocene, which suggest similar C
3
dietary and
energy sources. In general, the temporal spread of the data
reveals variability in dietary protein and dietary energy compo-
sition over the Holocene in the study region, with an emphasis
on C
3
protein/energy sources during the early and middle
Holocene and C
4
protein/energy sources during the initial and
final late Holocene.
Tabl e 4 ttest values and statistical significance for inter-sample mean
comparisons for δ
13
C
col
(below of the diagonal) and δ
13
C
ap
(above of the
diagonal)
EMH MH ILH FLHEM FLHLM
EMH 0 0.09 0.49 −19.4*** −14.1***
MH −1.31 0 0.26 −20.1*** −17.7***
ILH −4.70* −4.60* 0 −11.2*** −10.3***
FLHEM −24.1* −22.5* −5.3* 0 2.00**
FLHLM −24.9* −23.8* −4.0* −0.23 0
*p≤0.001, significant differences for δ
13
C
col
**p≤0.005, significant differences for δ
13
C
ap
***p≤0.001, significant differences for δ
13
C
ap
Tabl e 5 ttest values and statistical significance for inter-sample mean
comparisons for δ
15
N
col
(below of the diagonal) and Δ
13
C
col-ap
(above of
the diagonal)
EMH MH ILH FLHEM FLHLM
EMH 0 0.74 0.06 2.88** 3.86***
MH −1.38 0 0.06 1.26 2.93**
ILH −1.83 −0.51 0 0.63 1.80
FLHEM −7.1* −3.86* −2.85* 0 −2.70**
FLHLM −6.57* −4.73* 2.68* 5.7* 0
*p≤0.001, significant differences for δ
15
N
col
**p≤0.005, significant differences for Δ
13
C
col-ap
***p≤0.001, significant differences for Δ
13
C
col-ap
Fig. 3 δ
13
C
col
plotted against δ
15
N from Sabana de Bogotá human
samples for four chronological samples: early Holocene hunter-
gatherers (triangles), middle Holocene hunter-gatherers (circles), initial
late Holocene hunter-gatherers/horticulturalists (diamonds), and final late
Holocene agriculturalists (squares). aIndividual data points and bmean
values ± 1 standard deviation. Ninety-five percent confidence ellipses for
each chronological group are shown
Archaeol Anthropol Sci

Multivariate analysis
The results of the DFA are presented in Tables 6and 7and
Fig. 6. The k-means cluster analysis revealed the existence
of four main clusters with distinct multivariate dietary pro-
files. Only linear functions with higher variance and canon-
ical correlations were interpreted (i.e., functions 1 and
2 = 99.8 % of the total variance). The structure analysis
showed that carbon isotope variables have the heaviest in-
fluence on function 1, while nitrogen exerted its strongest
effect on function 2 (Table 6). The classification analysis
based on posterior probabilities and inter-individual
Mahalanobis distances (D
2
) revealed a very good corre-
spondence between the observed and predicted isotope-
based classification (only 0.07 % incorrect classifications).
The four clusters are plotted in Fig. 6, both as individual
data points (a) and multivariate centroids (b). Function 1
clearly differentiates between clusters with low (negative
scores) and high (positive scores) carbon values. Clusters
Fig. 4 Scatterplots of four stable isotopes against chronology raging between 9000 and 500 cal BP for human samples from the Sabana de Bogotá
region. aδ
13
C
col
,bδ
15
N
col
,cδ
13
C
ap
,anddΔ
13
C
col-ap
. Color codes as in Fig. 3
Fig. 5 δ
13
C
col
plotted against δ
13
C
ap
for five chronological samples from
the Sabana de Bogotá region according to the regression model of Kellner
and Schoeninger (2007). Early Holocene hunter-gatherers (triangles),
middle Holocene hunter-gatherers (circles), initial late Holocene hunter-
gatherers/horticulturalists (diamonds), and final late Holocene agricultur-
alists (squares). Color codes as in Fig. 3
Archaeol Anthropol Sci

1 (circles) and 2 (squares) are markedly different from clus-
ters 3 (diamonds) and 4 (triangles). This distinction has eco-
nomic sense, since clusters 1 and 2 correspond to hunter-
gatherers from the early, middle, and initial late Holocene
and clusters 3 and 4 correspond to final late Holocene agri-
culturalists. Function 2 allows us to distinguish between
clusters with low (negative scores) and high (positive
scores) nitrogen values. This differentiation can be ex-
plained in temporal terms since cluster 1 corresponds to
early Holocene hunter-gatherers with low nitrogen values
and cluster 2 comprises middle and initial late Holocene
hunter-gatherers with high values. The distinction between
clusters 3 and 4 based on function 2 (nitrogen) supports the
bivariate results (Fig. 3;Tables4and 5) suggesting that
people from the late Muisca period consumed higher
amounts of protein than their early counterparts. Overall,
the multivariate model suggests that early and middle
Holocene foragers presented ca. 100 % of C
3
diets and
≥65 % of C
3
protein sources, while final late Holocene ag-
riculturalists presented 70 % of C
4
diets and ∼50 % of C
4
protein sources. The high positive scores of some individ-
uals along function 2 suggest either the presence of marine
protein (see Somerville and Froehle 2011)orastrongfocus
on local freshwater fauna. Alternatively, the elevated nitro-
gen values could be at least partly attributed to the use of
animal fertilizers, burning of vegetation, and/or land man-
agement by the final late Holocene societies (see Szpak
2014). Finally, Table 7presents the matrix of D
2
distances
between the four dietary clusters, which revealed significant
differences between clusters 1–2and3–4 but not between 1
and 2 or between 3 and 4. This suggests that, in dietary
terms, cluster 1 (low carbon/low nitrogen), representing ear-
ly Holocene hunter-gatherers, is similar to cluster 2 (low
carbon/high nitrogen), which includes mid and initial late
Holocene hunter-gatherers/horticulturalists. Additionally,
clusters 1 and 2 are markedly different from clusters 3 (high
carbon/low nitrogen) and 4 (high carbon/high nitrogen),
which correspond to final late Holocene agriculturalists
from the early and late Muisca period, respectively.
Tabl e 6 Function eigenvalues and structure matrix
Structure analysis
Function Eigenvalue % of variance Cumulative % Canonical correlation δ
13
C
apatite
δ
13
C
collagen
δ
15
N
collagen
1 8.92 85.8 85.8 0.948 0.907* 0.882* 0.173
2 1.46 14.3 99.8 0.771 −0.273 −0.035 0.907*
3 0.01 0.2 100 0.125 −0.318 0.468 −0.384
*p≤0.01, significant canonical coefficients
Tab l e 7 Matrix of square Mahalanobis distances among clusters
(below of the diagonal D
2
values and above of the diagonal Fvalues
a
)
Group Cluster 1 Cluster 2 Cluster 3 Cluster 4
Cluster 1 0 17.4 134.5 156.5
Cluster 2 11.48 0 196.2 181.7
Cluster 3 59.31* 66.10* 0 35.24
Cluster 4 71.48* 64.10* 4.69 0
a
Fvalues = 3.1 d.f.
*p≤0.001, significant differences
Fig. 6 Discriminant function scores plotted by cluster representing four
multivariate dietary profiles as established by the discriminant function
analysis. Cluster 1 (circles), cluster 2 (squares), cluster 3 (diamonds), and
cluster 4 (triangles). aIndividual data points and bmultivariate centroids.
Error bands extend to 2σof the centroids. Ninety-five percent confidence
ellipses for each cluster are shown
Archaeol Anthropol Sci

Discussion: subsistence and dietary trends
at the Sabana de Bogotá
The isotopic evidence presented above revealed an important
transformation in diet and subsistence at the SB region over
time, which can only be assessed on wide archeological time-
scales (i.e.,millennia). Here, the dietary/subsistence trends are
addressed by temporal blocks roughly corresponding to pe-
riods of remarkable cultural change in the study region.
Early Holocene (ca. 9000–7000 cal BP)
Past interpretations on SB early hunter-gatherer subsistence
indicated dietary specializations (Correal and van der
Hammen 1977; Correal 1986;Hurtetal.1977;vander
Hammen et al. 1990), while recent studies tend to stress more
generalized diets and economies (Aceituno and Loaiza 2015;
Borrero 2015; Cárdenas 2002; Delgado 2015; Piperno and
Pearsall 1998). Much of the subsistence specialization (i.e.,
hunting) was inferred from the lithic assemblages; however,
the most important and ubiquitous late Pleistocene/early
Holocene regional lithic industry (i.e., Abriense) is not a bifa-
cial technology but a very simple, versatile, and multifunc-
tional unifacial technology that reflects environmental con-
straints rather than specializations (Delgado 2012a). Recent
technofunctional analysis revealed the existence of broad
spectrum economies with a strong focus on vegetal resources
(Nieuwenhuis 1998,2002). The isotopic results presented
here are in agreement with the recent interpretations of the
lithic repertoire indicating that early Holocene forager diets
were mostly integrated by C
3
plants. Although animal protein
was less important, it should be noted that this protein came
from diverse C
3
sources, which, in turn, indicates flexibility in
resource acquisition. The multivariate and regression analyses
(Figs. 5and 6; Table 6) strongly support this interpretation as
about 80–100 % of the dietary energy of early hunter-
gatherers came from C
3
vegetal sources. In addition, the tem-
poral dispersion of nitrogen and diet-apatite spacing (Fig. 4b,
d) stress that C
3
animal protein was also a relatively important
dietary component for some early foragers. This pattern is
supported by distinct lines of evidence. For example, the
archaeobotanical and lithic evidence highlights the impor-
tance of roots, tubercles, and seeds (Cárdenas 2002; Correal
and van der Hammen 1977; Nieuwenhuis 2002), and the
zooarchaeological record points todeer, guinea pigs, and other
small mammals as the main animal protein sources (Ijzereef
1978;PeñaandPinto1996). Bioarchaeological evidence in-
dicates abrasive diets and oral pathologies related to the high
consumption of minimally processed foods (Delgado 2015;
Gómez 2012). On the one hand, all this evidence indicates
that gathering was more important than hunting. On the other,
however, there was more dietary diversity than previously
assumed, which leads to the hypothesis of non-specialized
economies for early Holocene foragers.
The early Holocene was a period without marked environ-
mental changes in the SB region (Fig. 2). Likewise, aside from
a slight increase in carbon (collagen) and nitrogen during the
middle Holocene, the isotopic record shows overall relative
dietary stability between 9000 and 4500 cal BP, which means
that few significant changes occurred over millennia in con-
nection with subsistence (Fig. 4; Tables 4and 5). However,
individual data also suggest some interesting issues, especially
regarding mobility and the arrival of non-local populations.
The most conspicuous finding is the different dietary profile of
an early Holocene individual from Galindo site (Pinto 2003)
dated to 7730 ± 60 BP (GrN-16345) (8508 cal BP range 2σ
8406–8604), which presented a mixed C
3
/C
4
diet (see Figs. 3,
4,and5). Although some authors have pointed out that be-
cause this skeleton has not been directly dated, its unusual
carbon value (−15.3 ‰) could represent a late agricultural
individual unrelated to the dated stratum (Cárdenas 2002). A
distinct interpretation suggests that such individual could have
come from a lowland region and/or that it may have belonged
to a highly mobile group exploiting tropical resources fre-
quently. Recent analysis of dental and craniofacial morpholo-
gy suggests that during the early and middle Holocene, pop-
ulations with distinct phenotypic patterns could have arrived,
favoring the hypothesis of a non-local origin for such individ-
ual (Delgado 2015).
Some authors have suggested that the regional isotopic
record reflects the importance of logistic mobility (Cárdenas
2002;vanderHammenetal.1990) during the early Holocene,
given the allegedly clear signal of tropical C
4
plants and large
inter-individual isotopic variation (Cárdenas 2002). This,
along with the paucity of the archaeobotanical record for this
period, has led to interpret SB as a region for hunting rather
than gathering, where much of the vegetal resources come
from tropical lowlands (Cárdenas 2002). The results presented
here, excluding the Galindo individual, are not consistent with
the aforementioned hypothesis. On the contrary, they suggest
an entire homogeneous C
3
diet indicative of an intensive use
of locally available vegetal resources (Figs. 3,4,5, and 6;
Tables 3,4,5,and6). Additionally, the low preservation of
the paleobotanic remains may, in part, explain their alleged
absence in early contexts. Although the available isotopic ev-
idence is not very useful to discuss human mobility, it suggests
that early Holocene foragers exploited mostly local C
3
eco-
systems and had therefore a restricted geographic range. This
is partially supported by the paleoecological evidence, which
suggests a relatively homogeneous distribution of C
3
re-
sources over the early/middle Holocene for the SB (Boom
et al. 2001;MoraandPratt2002). Nevertheless, the finding
of both foreign fauna (e.g., Felidae and Atelidae families) and
non-local lithic tools (e.g., fluting technology) by using al-
lochthonous raw materials suggests that the widely accepted
Archaeol Anthropol Sci

territorial mobility hypothesis (e.g., Cárdenas 2002; Correal
and van der Hammen 1977) must bemonitored by using other
lines of evidence (Gnecco 2000).
Middle Holocene (ca. 6000–4500 cal BP)
The isotopic data for this temporal block shows few differ-
ences regarding the early Holocene, especially in terms of
carbon isotopes, which suggest a continuous exploitation of
local C
3
vegetal resources and that there was virtually no
change in gathering. Both the univariate/bivariate and
regression/multivariate analyses indicate strong dietary simi-
larity between early and mid-Holocene foragers (Figs. 3,4,5,
and 6; Tables 3,4,5,6and 7). The only change regarding the
previous period is a slight increase in nitrogen and diet-apatite
spacing, which indicates higher and more diverse animal pro-
tein consumption during the middle Holocene (Figs. 3and 4b;
Table 5). The zooarchaeological record indicates that small
mammals, such as guinea pigs, became more important than
deer during this time period. The increased importance of
Cavia porcellus over other animal resources (e.g., deer) for
middle Holocene hunter-gatherer economic strategies remains
unclear. From the perspective of evolutionary geography
(sensu Lahr and Foley 1998), the author (Delgado 2012a,
2015) suggested that mid-Holocene climatic changes (temper-
ature increase and aridity) may have caused significant eco-
logical modifications resulting from climate-dependent
chorological changes affecting vegetal and animal communi-
ties. Thus, the retraction and/or fragmentation of forested
areas likely produced the decline of deer populations, which,
in turn, allowed the more intensive use of guinea pigs and
other small-sized animals adapted to open habitats (i.e., grass-
lands) and freshwater resources. The relatively wide range of
nitrogen (Figs. 3and 4b; Table 3) seems to support this inter-
pretation since it suggests the consumption of relatively di-
verse animal protein sources during this period.
An important aspect that must be taken into account for the
interpretation of the emergence of agriculture in the study
region from the isotopic record is that despite the fact that
the most important changes related to food production are
more noticeable during the initial and final late Holocene
(e.g., the introduction of tropical crops, the intensive cultiva-
tion of C
3
plants, etc.), this does not necessarily imply that that
an early horticulture of C
3
plants was not developed, especial-
ly during the middle Holocene. The distinct analyses per-
formed here, both univariate/bivariate and multivariate reveal-
ing a strong emphasis on C
3
plants, seem to support a mid-
Holocene horticulture system (Figs. 3,4,5,and6; Tables 3,4,
5,and6). This is in agreement with the rich paleobotanical
record highlighting the importance of squash, Dioscorea,oca,
and other highland tubercles (Cárdenas 2002;Correal1990b;
Correal and van der Hammen 1977). In addition, the initial
appearance of lithic tools for vegetal processing in the local
archeological record dated to ca. 5800 cal BP (GrN-14477)
(range 2σ5560–5798) (Correal 1990b) also highlights the
intensification of plant use from the middle Holocene on-
wards. This is interesting, as similar kinds of lithic tools have
been found in archeological sites with clear and reliable evi-
dence of plant management, since the Pleistocene/Holocene
transition (Aceituno and Loaiza 2015;GneccoandMora
1997;Gnecco2003).
InitiallateHolocene(ca.3800–2200 cal BP)
The initial late Holocene is a crucial period to address plant
domestication and the origins of agriculture in the study re-
gion because it is during this period that some of the most
important changes in food production occurred. The results
of this study show the existence of C
3
,mixedC
3
/C
4
,andC
4
diets (Figs. 3and 4; Tables 3,4,and5). Although it is possible
that during this period groups and/or individuals with distinct
diets coexisted, this pattern also can be the result of poor
chronological resolution and small sample size. Thus, the tran-
sitional character of this period may change in the near future
with more and well-dated human samples. The extensive
archaeobotanical evidence recovered from Aguazuque (ca.
4300 cal BP) and Zipacón (3500 cal BP (GrN-11125) (range
2σ3445–3571), which includes sweet potato (Ipomoea
batata), calabash tree (Cresentia cujete), avocado (Persea
americana), cherry tree (Prunos serotina), and maize (grains
and cobs of Z. mays)(Correal1990b; Correal and Pinto 1983),
points out that by the initial late Holocene, SB populations
were already consuming several C
3
and C
4
domesticated
plants. Regardless of some fluctuations, isotopic information
suggests that the main dietary change occurred ca. 3000–
2800 cal BP, when people consumed significantly more C
4
plants and animal protein (Fig. 4). The chronological discrep-
ancy between the paleobotanic and the isotopic record regard-
ing the initial time of dietary change could be attributed to the
paucity of the isotopic evidence. Yet, the finding of two indi-
viduals from the upper levels of Tequendama dated around
3900–3500 cal BP and with carbon values indicative of mixed
C
3
/C
4
diets (see Fig. 4a) shows that actually a date of ca.
4000 cal BP may more reliably represent the initial change
toward a C
4
diet. Bioarchaeological analysis supports the di-
etary change inferred from the isotopic and archaeobotanical
record, since it indicates, on the one hand, an important in-
crease in oral pathologies such as caries, dental calculus, and
enamel hypoplasias and, on the other, the reduction of occlu-
sal dental wear rates (Delgado 2015). The results also showed
a slight increase in nitrogen (Fig. 4b), which coincides with
the preponderance of guinea pig remains, highlighting the
economic importance of this species for late Holocene horti-
cultural societies (Correal and van der Hammen 1977; Correal
and Pinto 1983; Correal 1990b). This is interesting because on
the basis of the analysis of skeletal morphology, Correal and
Archaeol Anthropol Sci

Pinto (1983, p. 183) suggested that the probable date for the
initial domestication of this species is around 3500 cal BP,
which supports previous proposals (Ijzereef 1978,p.170)that
state that by ca. 2600 cal BP, these animals had been fully
domesticated.
One of the main goals of this research was to provide in-
terpretations about the biocultural processes that might have
allowed the cultivation of plants. I also attempted to under-
stand whether these biocultural processes were promoted by
external factors such as climatic changes and/or population
dispersals or whether they were the product of an in situ de-
velopment. After evaluating the temporal dispersion of the
isotopic record (especially carbon isotopes) throughout the
Holocene (Figs. 4and 5; Tables 3and 4) by using distinct
statistical and graphical approximations, the most conspicu-
ous patterns are (1) homogeneity of the C
3
signal between
9000 and ca. 4500 cal BP; (2) the presence of C
3
,C
3
/C
4
,
and C
4
diets between ca. 4000 and 3500 cal BP; and (3) the
preponderance of the C
4
signal after 2000 cal BP (Figs. 3,4,5,
and 6; Tables 3,4,and5). Despite the fact that in situ devel-
opment of agriculture is likely, especially given the impor-
tance of vegetal resources for the hunter-gatherer economy
during the early and middle Holocene, the occurrence of
strong, rapid, and multiple biocultural changes suggests that
other factors were likely involved, with the most relevant be-
ing the entry of non-local populations with an agricultural
subsistence. Climate change and environmental rearrange-
ments do not seem to have been an important factor prompting
to subsistence changes as the paleoecological record shows
only a slight increase in precipitation and humidity during this
time span (Marchant et al. 2002). In this context, it is worth
mentioning the findings concerning the earliest evidence of
maize and ceramic technology in the study region dated to
around 3500 cal BP (Correal and Pinto 1983). Such evidence
suggests, on the one hand, that despite the fact that maize
could have been introduced well before 3500 cal BP given
the early evidence of maize in other regions of northwestern
South America (Bray et al. 1987; Cavelier et al. 1995;
Monsalve 1985), its role as the mainly consumed plant took
place later. On the other hand, it is striking that the earliest
evidence of maize appeared along with the oldest evidence of
pottery related to non-local lowland populations (Botiva
1989), which points to the fact that some of the most important
cultivated crops may have been introduced by population ex-
pansions. This is in line with the long-held view of local
archeologists, who have favored the hypothesis that incipient
agriculture was introduced by populations from the
Magdalena valley at least since ca. 3500 cal BP (Ardila
1984; Botiva 1989; Correal and Pinto 1983). Even though
the isotopic record is fairly incomplete, it suggests similar
dates for the initial dietary change around ca.4000 cal BP
(Figs. 3and 4). This is relevant since studies of craniofacial
and dental morphology found remarkable evolutionary
diversification during the initial late Holocene indicating pop-
ulation discontinuity (Delgado 2012a,b,2015; Rodríguez and
Colantonio 2015). Together, this data indicate that the change
from C
3
diets related to hunter-gatherers/early horticulturalist
to C
4
diets characteristic of agricultural societies is concomi-
tant with the appearance and dispersals of food processing
technologies (pottery and gridding tools) and the entry of hu-
man populations with distinct phenotypic patterns.
Accordingly, these lines of evidence strongly support previous
hypothesis that non-local populations, likely from the
Magdalena valley, with distinct behavioral and biological
traits introduced the tropical crop agriculture to the SB region
during the initial late Holocene (Correal and van der Hammen
1977;Correal1990b).
Final late Holocene (ca. 1300–600 cal BP)
The archeological record along with ethnohistorical accounts
show that the Muisca society introducedintensive agriculture,
developed advanced agricultural strategies, and established
wide and complex commercial networks, all of which implied
the availability of different foodstuffs from several regions
(Cárdenas 1996; García 2012; Kruschek, 2003; Langebaek
1987). The isotopic record coincides with this diverse picture
as it shows the existence of relatively heterogeneous diets and
a well-established agriculture during the Muisca period, with
some differences between the early and late period. The bio-
chemical evidence stresses the importance of C
4
plants (pri-
marily maize) complemented with other C
3
and C
4
crops, as
well as C
4
-feeding animals and freshwater resources (Figs. 3,
4,5,and6; Table 2). Although the strong C
4
signal suggests
that maize was the most commonly used tropical plant, other
C
4
crops (e.g., manioc), fruits, and palms were likely incorpo-
rated into the Muisca diet (García 2012). This means that the
overwhelming C
4
signal, which until now has been interpreted
as maize, in fact reflects more than one tropical resource con-
sumed by these societies corroborating the ethnohistoric evi-
dence (Langebaek 1987).
Previous studies (Cárdenas 1993,1996) emphasized the
absence of Andean foodstuffs in the isotopic record such as
highland tubers like potato (Solanum tuberosum), sweet pota-
to (I. batata), arracacha (Arracacia xanthorrhiza), oca
(O. tuberosa), mashua (Tropaeolum tuberosum), and ullucu
(Ullucus tuberosus), which according to etnohistoric evidence
were of crucial importance within the Muisca diet (Langebaek
1987). However, the bivariate results contradict such interpre-
tation, showing instead wide ranges for δ
13
C
col
(Fig. 3;
Tables 3and 4), where a large part of the Muisca sample
averaging ca. −15 ‰indicates that C
3
resources such as high-
land tubers were also commonly consumed. Similarly, the
regression and DFA results (Figs. 5and 6) point out a C
3
trend
for some individuals from the early and late Muisca period.
What is clear from the isotopic data is that C
3
plants were not
Archaeol Anthropol Sci

as important as C
4
crops during this time span (Figs. 4aand5).
Interestingly, the local isotopic ecology (Table 2)revealedthat
some animal species (e.g., guinea pig and rabbit) possessed
relatively enriched carbon isotopes, which is explained by the
presence of wild C
4
plants in the SB region during the final
late Holocene (Mora and Pratt 2002; supplementary Table 2).
This implies that humans feeding on those animals may have
displayed the same phenomenon. These data suggest that the
alleged carbon enrichment along with the use of several C
4
products might overshadow the isotopic signal of C
3
plants.
Some researchers documented a sociopolitical differentia-
tion between the early and the late Muisca periods (Boada
2006; Henderson and Ostler 2005; Kruschek 2003), which
coincides with other behavioral aspects, including socially
constituted food consumption practices. Here, carbon and es-
pecially nitrogen isotopes revealed some differences between
both periods. The bivariate results (Figs. 3a, b and 4b–d) show
that the sample from the late period present higher nitrogen
values, while the sample from the early period present slightly
higher carbon ones; some of these differences are statistically
significant (Tables 4and 5). In addition, the DFA results sup-
port such chronological differentiation (Fig. 6; Tables 6and
7). For carbon isotopes, cluster 3 (mostly representative of the
early period) shows slightly more negative values indicating
the relative importance of C
3
resources. For nitrogen, cluster 4
(mostly representative of the late period) shows higher values,
which suggests more protein intake, primarily from animal
sources (see also Fig. 4b). Cárdenas (1993) interpreted the
relatively high nitrogen values in Muisca samples as evidence
of marine resource consumption. In line with this, there have
also been findings of marine animal remains (mollusks, gas-
tropods, and shells) and the circulation of exotic marine prod-
ucts such as salt, fish flour, and salted and smoked fish within
theMuiscaterritory.However,Cárdenas(1993,1996)errone-
ously interpreted the high nitrogen values in infants of 0–
3 years old (which are related to breastfeeding actually) as
indicative of marine resources. His suggestion regarding the
circulation and consumption of exotic marine products is
problematic because these resources are not well-represented
in the isotopic record. Despite the absence of a highly devel-
oped isotopic ecology, especially for local aquatic habitats, the
results presented here suggest that the relatively high nitrogen
values can be explained by the consumption of freshwater
resources (e.g., fish), especially given the vast
zooarchaeological evidence for the late period indicating the
intensive exploitation of such resources (Enciso 1996).
Taking into account the entire temporal range investigated
(ca. 9000–600 cal BP), it is clear that some of the most im-
portant changes regarding diet, according to the stable isotope
data analyzed (Figs. 3,4,5,and6; Tables 3,4,5,6,and7),
occurred during the late Holocene and more specifically, dur-
ing the Muisca period. Such dietary change and its associated
biocultural transformations had profound implications for the
health and behavior of the Muisca societies. Complementary
bioarchaeological evidence revealed that during the final late
Holocene, there was an increase in the rate and plane of oc-
clusal dental wear potentially related to the intensive use of
grinding stones for processing plants. This infused additional
environmental grit into the meal in the form of stone chips
from the grinding implements producing more pronounced
dental wear (Delgado 2015). Increased focus on maize, indi-
cated for the strong C
4
signal (Figs. 3,4,5,and6), could have
negative consequences on the health of Muisca populations
given its association with pathologies that result in iron defi-
ciency, such as porotic hyperosthosis and criba orbitalia.
Despite the fact that recent studies suggest more complex
etiologies for such diseases (Walker et al. 2009), it is interest-
ing that some authors reported higher frequencies among
Muisca populations compared to other periods (Martínez
2012;Rodríguez2006). Coinciding with the increased maize
consumption, there is an increase in the prevalence of carious
lesions over the course of the Muisca period (Delgado 2015).
Finally, the analysis of dental enamel hypoplasias and non-
specific infections (periosteal reactions) provides further evi-
dence that Muisca populations may have experienced a dra-
matic increase in physiological stress (Delgado 2015;
Rodríguez 2006). In general, the introduction of intensive ag-
riculture produced a decline in health for the Muisca popula-
tions that reflects a change in the quality of diet and lifestyle.
Concluding remarks
The isotopic record revealed a slow subsistence transforma-
tion between the early and middle Holocene (∼9000–4500 cal
BP), which suggests dietary stability. Contrary to the expecta-
tions of a well-known model on Paleoindian subsistence, early
Holocene hunter-gatherers presented a strong focus on plants
with some fluctuation in protein sources (i.e., flexibility). The
noticeable biocultural and climatic changes that occurred dur-
ing the middle Holocene (ca. 6000–4500 cal BP) contrast with
the stable isotope data only pointing to a slight increase in
protein consumption. The appearance of lithic tools for inten-
sive vegetal processingand the finding of somecultigens sug-
gest that C
3
plant horticulture emerged during the middle
Holocene. However, it is ca. 4000 cal BP when a change
toward mixed C
3
/C
4
diets occurred. Around ca. 3500 cal BP,
human populations presented a strong C
4
signal and a slight
increase in protein consumption. During the Muisca period
(last 1100 cal years BP), the agricultural societies exhibited a
strong reliance on C
4
plants such as maize complemented with
other C
3
and C
4
crops, C
3
-C
4
feeding animals, and freshwater
resources. In addition, there were differences in animal protein
and C
3
plant consumption between early and late Muisca
samples indicating slight changes in subsistence in the SB
region in the previous European contact. Lastly, although this
Archaeol Anthropol Sci

research revealed interesting issues on the evolution of diet
over the Holocene in this region, further research is still re-
quired. New stable isotope measurements for important pe-
riods (e.g., initial late Holocene) are necessary, which include
additionaldata on mobility and dietary mobility along with an
enhancement of the chronological resolution and a more com-
plete regional isotopic ecology reconstruction.
Acknowledgments I would like to thank German Mora and Arnoud
Boom for sharing their data on carbon isotopes from paleoenvironmental
researches. Thanks to Javier Giraldo (Universidad del Cauca, Colombia)
and Alejandra Ortíz (Arizona State University, USA) for their useful
comments on early drafts of this paper. Thanks to Alexandra Delgado
for help with the English version of the manuscript. This research was
partially supported by the Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET, Argentina) and Fundación de
Investigaciones Arqueológicas Nacionales (FIAN, Colombia) (project
no. 409-2010).
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