ELECTRON_SPIN_RESONANCE_DATING_OF_TOXODO

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Radiation Protection Dosimetry (2016), pp. 1–6 doi:10.1093/rpd/ncw195
ELECTRON SPIN RESONANCE DATING OF TOXODON TOOTH
FROM UPPER RIBEIRA VALLEY, SÃO PAULO, BRAZIL
Angela Kinoshita1,2,6,*, Aline Marcele Ghilardi3, Marcelo Adorna Fernandes4, Ana Maria G. Figueiredo5
and Oswaldo Baffa2
1Universidade do Sagrado Coração (USC), Bauru, São Paulo, Brazil
2Departamento de Física, FFCLRP, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil
3Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Rio de Janeiro, Brazil
4Universidade Federal de São Carlos (UFSCar), São Carlos, São Paulo, Brazil
5Instituto de Pesquisas Energéticas e Nucleares, IPEN-CNEN, São Paulo, Brazil
6Present Address: Rua Irmã Arminda 10-50, Bauru, SP 17.011-160, Brazil
*Corresponding author: angelamitie@gmail.com
Electron spin resonance (ESR) dating was applied to date a sample of fossil tooth found in Ribeira Valley, São Paulo, Brazil. This
region is characterized by abundant fossil records of Pleistocene–Holocene South American megafauna belonging to different faun-
istic moments related to climate changes during the quaternary. As the number of fossils dated is not too large, the dating of mate-
rials from this region will provide important information to better understand the events associated with the presence and
extinction of these species. The equivalent dose (De) was determined using single exponential fitting resulting in (24 ± 1)Gy. The
De was converted to age using ROSY ESR Dating program and the concentration of radioisotopes present in the sample and soil
determined through neutron activation analysis. The ages cover the range of 25–34 ka. This information is important to contextual-
ize other findings in the region from different sites and to help obtain better information about the climate changes in this region.
INTRODUCTION
The region known as the Upper Ribeira comprises
the southeastern part of São Paulo State, southeast
Brazil, and is included in the Iguape River Basin.
The area is characterized by its geological complex-
ity and karst development, which houses an exten-
sive system of caves. Quaternary sediments, from the
Pleistocene–Holocene period, are associated with
these underground cavities and often preserve fossils.
The absence or low concentration of collagen in the
megafauna remains found in some types of soil can be
the main limitation to radiocarbon dating(1–4) hamper-
ing the scientific determination of its chronology. In
these conditions, dating by electron spin resonance
(ESR) represents an alternative for reconstructing the
chronology of the presence of species(1–3), making it
possible to investigate several aspects related to the
quaternary megafauna.
ESR dating, as well as thermoluminescence (TL)
and optically stimulated luminescence (OSL) are
based on the effects of ionizing radiation in solids.
Ionizing radiation is produced by natural radioactive
elements such as 238U, 232Th and 40K present in the
environment and/or in the archeological material
itself, and by cosmic radiation. ESR dating can be
applied to any solid insulator, but fossil tooth is the
material most commonly dated by this technique,
given its current development(5).
The main radical generated in hydroxyapatite that
is used for dose determination is the CO2
− derived to
the presence of carbonate impurities (CO3
2−) in the
hydroxyapatite (Hap) matrix. This radical has an
estimated lifetime of 107 y (25°C) which allows its
use for archeological dating(5, 6). The calibration of
the ESR spectra intensity as a function of the dose is
made by the additive dose method. The idea is that
if it is possible to know the concentration of defects
(i.e., the stable free radicals in the carbonate impur-
ities) associated with adding known doses to the
sample, the rate of change in defects per known
added gray may then be used to estimate the time
elapsed until the present concentration was achieved.
Thus, additive known doses are applied in the
laboratory to produce additional defects. The inten-
sity of the spectrum is determined for each dose
enabling the construction of an additive dose-
response curve. Usually, the curve of the intensity
signal ESR to the dose is adjusted by a single satur-
ation exponential curve (SSE), a SSE plus linear
curve and even a double exponential for very old
samples(5, 7). In the present case, the single satur-
ation curve seems to be the most appropriate method
because when comparing with a SSE plus linear,
SSE does not overestimate the dose:
= { − } ( )−[( + ) ]I I e1 , 1D D D0 /e 0
where I is the ESR signal intensity, D the additive
dose, I0 and D0 are the intensity and dose,
respectively, in the saturation and De the equiva-
lent dose.
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The accumulated dose in sample De is converted
into age through the internal and external dose rate.
As already mentioned, these doses are produced by
natural radioactive elements present in the environ-
ment and /or in the archeological material itself and
by cosmic radiation. The internal dose rate depends
on the way in which the Uranium has been incorpo-
rated in the material. In the case of teeth, there are
models that have been implemented in software,
such as ROSY(8) and DATA(9). The models
are called Early Uptake(10), where it is assumed that
the incorporation occurs in the early stages after the
burial; Linear Uptake(11), when the incorporation is
linear with time and Recent Uptake, when it is
assumed that this uranium is incorporated at a time
close to sample collection. The last provides the
maximum age of the sample(12). The Uranium
uptake history can be determined by solving the
equation proposed by Grun et al.(13) coupling the U-
series to ESR. This methodology has been applied
successfully in several problems(14–17) and it is
important when the ages are great and the difference
between the ages obtained by using the models pre-
viously mentioned are very large.
When the data required to apply the ESR U-series
are not available, the ESR age may be considered
between EU and RU age.
ESR dating has been successfully employed to
date fossil samples from Pleistocene mammals from
deposits of cacimbas or tanques(18–21), deposits of
karst systems(22, 23) bones from Sambaquis(24) and
teeth from submerged deposits and fluvial sys-
tems(1, 2, 25, 26). Following on these studies, in this
work ESR dating has been applied to a tooth found
in this region.
MATERIAL AND METHODS
Geographic and geological settings
The fossil tooth used in this study was collected in
2008 in Los Tres Amigos Abyss, Bulha d’Água
region, Intervales State Park (coordinates: 24°0′21″S
48°20′58″W) (Figure 1). Figure 2 is a photograph
of a fossil found in this site. As it is common for
the cave deposits of this region, there is no strati-
graphic information about the fossil, since the qua-
ternary sediments are constantly reworked by floods,
which destroy the stratigraphic stacking and mix the
fossiliferous horizons(27).
ESR dating
Figure 2 is a photograph of the Toxodon tooth
studied in this work. The soil associated with the
sample was used to determine the radioisotopes
238U, 232Th and 40K. The enamel layer was sliced
with a carbide disk driven at low speed motor,
under constant irrigation with water to prevent
heating. Later, the enamel was easily separated out
from the dentin.
Next, the enamel layer was subjected to an acid
treatment (HCl) 1:5 in ultrasonic bath for 1 min to
extract an outer layer, both faces. The thickness
before treatment was about 1.2 mm and after treat-
ment, 1.0 mm
After drying, theenamel was manually ground in
an agate mortar to a powder with particle diameter
ϕ < 0.5 mm.
Dentin and the associated soil were also crushed.
The soil associated with tooth was sampled in three
aliquots and, together with the enamel and dentine,
Figure 1. Ribeira Valley map showing the Açungui Group
karst area, its main fossiliferous localities and the Apiaí
and Iporanga municipalities.
Figure 2. Fossil tooth of Toxodon. The enamel layer was
easily removed from the sample.
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were subjected to neutron activation analysis (NAA)
to determine the concentrations of 238U, 232Th and
40K.
The spectrum of powdered enamel was recorded
using Jeol X-Band (FA 200) spectrometer and com-
pared to a sample of non-fossilized bovine enamel,
previously irradiated with a known dose (150Gy) for
preliminary evaluation of the accumulated dose
(De), allowing the planning of added doses applied
to aliquots of fossil sample. Subsequently 10 aliquots
of about 70 mg were selected and each aliquot was
irradiated with different doses of gamma rays from
Cobalt-60 source, ranging from 0 to 200 Gy.
The spectra were recorded with the following set-
tings: microwave power 2 mW, below the signal sat-
uration, scan width 10mT, scan time 1min,
modulation amplitude 0.1 mT, modulation frequency
100 kHz, time constant 100ms. The dose-response
curve was constructed using the peak-to-peak inten-
sity of the ESR signal g⊥ and using single saturation
exponential function [1] De was determined.
This result was converted into age, through the
ROSY ESR Dating program(8) using the concentra-
tion of radioisotopes present in the sample and in
soil. The value of 240 μGy/y was adopted for cos-
mic radiation dose rate, found after correction tak-
ing into account the latitude, longitude and altitude
of the location for the sample(28). The humidity was
measured and is approximately 40%. The values of
initial ratio U-234/U-238 of 1.2 and alpha efficiency
αeff = 0.13 were employed. It is interesting to note
that using more recent developed software as
DATA and ESR-US to obtain the age, the same
result was obtained with DATA and the ESR-US
age assuming the ratio for U-234/U-238 and letting
the Th-230/Th-234 vary from 0.1 to 0.22, an age of
31 ± 3 ka was found.
RESULTS AND DISCUSSION
Figure 3 shows the dose-response curve. The experi-
mental data points were fitted with Equation (1)
using the instrumental weighing to determine De
(29).
Table 1 shows the results of NAA for U, Th and K
performed in the enamel, dentine and soil. The results
for soil corresponds to the average and standard devi-
ation of three aliquots. Table 2 lists the internal and
external dose rates, calculated through the ROSY
ESR dating software(8). Table 3 summarizes the
values of Age, according to the Uranium Uptake
model, that is, Early Uptake (E.U.), Linear Uptake
(L.U.) and a Combination Uptake, that as set with
the models E.U. to dentin and L.U. to enamel due to
the difference in porosities.
Usually the age provided by Combination
Uptake model is adopted as being the most likely.
However, considering the uncertainty of the results,
it can be seen that the ages provided by the three
models are close and cover the range of 25–34 ka. It
is interesting to note that using the more recently
developed software (DATA(9) and ESR-US) to
obtain the age, the same result was obtained with
both, i.e., assuming the ratio for U-234/U-238 and
0 50 100 150 200
0.0
0.1
0.2
0.3
0.4
0.5
0.6
E
S
R
 s
ig
na
l a
m
pl
itu
de
 (
a.
u.
)
Dose (Gy)
Figure 3. Dose-response curve of sample. The experimental
data points were fitted by Equation (1).
Table 1. Concentration of 238U, 232Th and 40K in enamel,
dentine and soil associated to sample obtained through
NAA.
238U (ppm) 232Th (ppm) 40K (%)
Enamel 0.087 ± 0.01 <0.01 <0.075
Dentine 14 ± 2 <0.01 <0.075
Soil 2.9 ± 0.4 4.3 ± 0.7 0.30 ± 0.06
Table 2. Internal and external dose rates.
Internal (µGy/y) External (µGy/y)
Model α β β γ + cosmic
Early 13.02 4.45 183.09 652.95
Linear 5.84 2.09 118.85 652.95
Combination 13.39 4.53 118.78 652.95
Table 3. Age results according to Uranium uptake model.
De (Gy) E.U. (ka) L.U. (ka) C.U. (ka)
24 ± 1 28 ± 3 31 ± 3 30 ± 3
E.U., Early Uptake; L.U., Linear Uptake; C.U.,
Combination Uptake.
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letting the Th-230/Th-234 vary from 0.1 to 0.22, an
age of 31 ± 3 ka was found.
The result supports the hypothesis, the paleofau-
nistic assemblage of Ribeira Valley belongs to Late
Pleistocene–Holocene age. It also contributes to the
understanding of the local biochronology of an
extinct taxon.
Other Toxodon teeth dated from Ribeira Valley
were from Ponta de Flecha and Fóssil Abyss. They
were dated through ESR to average ages between
6.5 ka BP(23) and 13.6 ka BP through AMS(30) by
Hubbe et al. The age difference between two meth-
ods cannot be easily explained, but it appears that
ESR may have reached its limits of applicability and
probably the error range increases for such small De.
Therefore, it is difficult to distinguish between the
estimates of 6.5 and 13.6 ka even though this may be
a crucial issue for deciding whether megafauna were
present or not during the Holocene period.
Moreover, it is important to say that, due to using
a very conservative approach, just a small part of the
tooth enamel was analyzed resulting in a middle
Holocene age of ~6.5 ka. The other two parts of this
sample were sent by Neves and coworkers for AMS
dating. One of the samples had poorly preserved col-
lagen but even so the 13C/12C ratio was considered
reliable enough to produce an age of 13.6 y BP.
Therefore it is acknowledge that this particular
sample cannot be considered the final word. In par-
ticular, the criticism of Hubbe et al.(30) is based on
the mistaken assumption that ESR age was done in
bone. It is important to emphasize that in this work
these dates are based on tooth enamel and not bone.
For bones, it is well known that, since they are an
open system permeable to the leaching in and out of
radioisotopes such as U, Th and K, it is not yet pos-
sible to have precise information about the internal
dose, and hence it is agreed that bones cannot be
dated by ESR. This fact is pointed out by the paper
published by Skinner(29). However, this same paper
shows that, for tooth enamel, ESR dating is as reli-
able as other available techniques and should not be
considered an ‘experimental’ technique.
All ages related in Kerber 2011(25) fit well in the
chronology of the region as well as other works
that have shown ESR ages correlating well with
dates obtained by other methods(31–36). When com-
paring 14C with other dating methods based on the
effect of ionizing radiation on matter, such as TL,
OSL and ESR, it is obvious that the second group
of methods is more complex. ‘Trapped charge
methods’ (TL, OSL and ESR) depend on sample
environment. Barring contamination, 14C does not
suffer this complication, and generally can success-
fully use a smaller sample for testing. Thus, it is
also obvious that if a given sample has carbon it
should be first studied with 14C. However, there are
many samples that do not have carbon; there may
be contamination; or the sample may be older than
the limits of 14C. Other methods must then be tried
and the investigators must be willing to sacrifice a
good tooth to get the best dating.
The material presented here appears to be the old-
est Toxodon record from the Ribeira Valley, suggest-
ing that the presence of the taxon in the region
should be extended for about another 16 ka. Untilthe present study, the oldest material dated for
Ribeira Valey was a Glyptodon osteoderm, which
estimated to be approximately 21 ka.
Further Toxodon material from Brazil is dated
from Piauí (associated charcoal)(37), and Rio Grande
do Sul(25), obtaining ages of 11.6 and 19 ka BP
respectively. This also makes the present record
potentially the oldest Toxodon registered in Brazil,
increasing the knowledge regarding the chronology
of the Brazilian Pleistocene mammals. The oldest
ages for Pleistocene mammals are still found in
Minas Gerais (Hoplophorus, Pampatherium and
Paleolama, between 63 and 310 ka—U/Th from
speleothems).
ACKNOWLEDGEMENTS
To Carlos Brunello and Lourenço Rocha for tech-
nical assistance, Professor Maria Elina Bichuette,
Laboratório de Estudos Subterrâneos (LES)
Universidade Federal de São Carlos for providing
the sample, Instituto de Pesquisas Energéticas e
Nucleares (IPEN) for the irradiation of the samples.
The authors thank the two reviewers for helpful
comments and, in particular, the calculations of the
ESR/US age by reviewer #2 and Dr Ann Barry
Flood for her kindness to review the English
language.
FUNDING
This work was partially supported by Fundação de
Amparo à Pesquisa do Estado de São Paulo
(FAPESP), Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) and Conselho
Nacional de Desenvolvimento Científico e
Tecnológico (CNPq).
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	Electron Spin Resonance Dating of Toxodon Tooth from Upper Ribeira Valley, São Paulo, Brazil
	Introduction
	Material and Methods
	Geographic and geological settings
	ESR dating
	Results and Discussion
	Acknowledgements
	Funding
	References