YQRES-03378; No. of pages: 5; 4C:
Quaternary Research xxx (2012) xxx–xxx
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Quaternary Research
journal homepage: www.elsevier.com/locate/yqres
Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian
Intertropical Region
Mário André Trindade Dantas a, b,⁎, Rodrigo Parisi Dutra a, b, Alexander Cherkinsky c, Daniel Costa Fortier b,
Luciana Hiromi Yoshino Kamino d, Mario Alberto Cozzuol b, Adauto de Souza Ribeiro e, Fabiana Silva Vieira e
a
Programa de Pós-graduação em Ecologia, Conservação e Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade Federal de Minas Gerais,
Belo Horizonte, MG, Brazil
b
Laboratório de Paleozoologia, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil
c
Center for Applied Isotope Studies, University of Georgia, Athens, GA 30602, USA
d
Programa de Pós-Graduação em Biologia Vegetal, Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-010, Belo Horizonte, MG, Brazil
e
Departamento de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de Sergipe, Av Marechal Rondon s/n, Bairro Rosa Elze, CEP 49100-000, São Cristovão, SE, Brazil
a r t i c l e
i n f o
Article history:
Received 8 April 2012
Available online xxxx
Keywords:
Megafauna
Brazilian Intertropical Region
Carbon isotopes
AMS
a b s t r a c t
During the Pleistocene a fauna composed of large (biomass>44 kg) and giant mammals (biomass>1000 kg)
that are usually associated with open environments lived in the Brazilian Intertropical Region. We present
here new information concerning the paleoecology and chronology of some species of this megafauna. Carbon
isotope analyses were performed for a better understanding of the paleoecology of the species Eremotherium
laurillardi (Lund, 1842), Notiomastodon platensis (Ameghino, 1888) and Toxodon platensis (Owen, 1849). The
δ13C data allow attributing a generalist diet to these species, which varied according to the kind of habitat in
which they lived. In more open habitats all species were grazers; in mixed habitats E. laurillardi and T. platensis
were mixed feeders, and N. platensis was grazer; and in more closed habitats all species were mixed feeders.
© 2012 University of Washington. Published by Elsevier Inc. All rights reserved.
Introduction
The Brazilian Intertropical Region (BIR: sensu Cartelle, 1999) is characterized by the presence of several endemic giant mammals, which
lived during the end of the Pleistocene and beginning of the Holocene.
The BIR includes all states of the northeastern Brazil (except Maranhão)
as well as Goiás, Minas Gerais, Espírito Santo and Rio de Janeiro states
(Fig. 1).
According to Cartelle (1999), some species from the southern
regions of the continent (allochthonous fauna) would have migrated
to the BIR at the end of the Pleistocene and beginning of the Holocene.
In the BIR, these species would have coexisted sympatrically with the
autochthonous fauna of this region, which was adapted to live in dry
forests (savannah or steppic savannah). However, chronological data
gathered by Dantas et al. (2011) suggested that this fauna was not
restricted to the end of the Pleistocene as previously considered and,
therefore, they questioned the traditional interpretation regarding the
paleoecology of these faunas. The main purpose of the present contribution is to show and to discuss stable carbon isotope and radiocarbon
data for Eremotherium laurillardi (Lund, 1842), Notiomastodon platensis
⁎ Corresponding author at: Programa de Pós-graduação em Ecologia, Conservação e
Manejo da Vida Silvestre, Av. Antônio Carlos, 6627, CEP 31270-010, Universidade
Federal de Minas Gerais, Belo Horizonte, MG, Brazil.
E-mail address: [email protected] (M.A.T. Dantas).
(Ameghino, 1888) (=Stegomastodon waringi; Mothé et al., in press)
and Toxodon platensis (Owen, 1849) from some localities of the BIR.
Materials and methods
Sixteen skeletal samples of Eremotherium laurilardi, N. platensis, and
T. platensis from localities in Bahia (BA), Sergipe (SE) and Rio Grande do
Norte (RN) (Table 1) were measured to obtain the carbon isotopic composition of bone, dentin and enamel carbonate. Some of these samples
(Table 1) were dated using accelerator mass spectrometry (AMS) at
the Center for Applied Isotope Studies of the University of Georgia/
USA, calibrated using IntCal98 (Reimer et al., 2009). Samples were collected from fossil specimens housed at the following institutions:
Laboratório de Geologia/Universidade Estadual do Sudoeste da Bahia
(Bahia, Brazil); Laboratório de Paleontologia/Universidade Federal de
Sergipe (Sergipe, Brazil); Memorial de Sergipe/Universidade Tiradentes
(Sergipe, Brazil); and Museu Câmara Cascudo/Universidade Federal do
Rio Grande do Norte (Rio Grande do Norte, Brazil).
Data from the 13C analyses (δ 13C ‰) were used to infer the diet of
the studied mammals. In medium- to large-sized animals δ 13C can be
enriched by 12‰ to 14‰ (Cerling and Harris, 1999). Values of
δ13C b −10‰, which were found in the tooth enamel, represent a pure
C3 feeder, whereas values of δ13C >−1‰ represent a diet based on C4
grasses. Values of δ13C between −10‰ and −1‰ indicate a mixed
0033-5894/$ – see front matter © 2012 University of Washington. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.yqres.2012.09.006
Please cite this article as: Dantas, M.A.T., et al., Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical
Region, Quaternary Research (2012), http://dx.doi.org/10.1016/j.yqres.2012.09.006
2
M.A.T. Dantas et al. / Quaternary Research xxx (2012) xxx–xxx
Figure 1. Brazilian Intertropical Region (BIR) map, showing the potencial distribution of the Atlantic Forest (modified from Carnaval and Moritz, 2008) and the Dry Tropical Forest (after
Werneck et al., 2011). (A) Represents a region which includes the municipalities of: Vitória da Conquista/BA, Morro do Chapéu/BA, Ourolândia/BA, Quinjingue/BA, and, tentatively, Toca
do Gordo do Garrincho/PI (?), Águas de Araxá/MG (?) and São José do Itaboraí/RJ (?). (B) Region that includes the municipalities of Coronel João Sá/BA, Poço Redondo/SE, Gararu/SE,
Canhoba/SE and Maravilha/AL. (C) Region that includes the municipalities of Rui Barbosa/RN, Barcelona/RN and Currais Novos/RN. States that comprise the BIR: GO — Góias; MG — Minas Gerais;
RJ — Rio de Janeiro; ES — Espirito Santo; BA — Bahia; SE — Sergipe; AL — Alagoas; PE — Pernambuco; PB — Paraíba; RN — Rio Grande do Norte; CE — Ceará; PI — Piauí (sensu Cartelle, 1999).
diet of C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005).
These values were here considered in the interpretation of isotopes
values for both bone and dentin. Examples of recent studies with this
approach were conducted by MacFadden et al. (1999) for Equus;
Sánchez et al. (2004) for Notiomastodon and Cuvieronious; and
MacFadden (2005) for Toxodon and Mixotoxodon.
Table 1
13
C analyses and radiocarbon dating for skeletal elements of Brazilian Intertropical Region fossils. Legends — skeletal tissue (st): d (dentine); b (bone); or e (enamel).
Species
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Eremotherium laurillardi
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Notiomastodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Toxodon platensis
Sample number
(3)
UGAMS 4935
UGAMS 4936(3)
SM-1(1)
MA-1(1)
UGAMS 4931(3)
UGAMS 4932(3)
UGAMS 4933(3)
UGAMS 4934(3)
UGAMS 6136(2)
UGAMS 4940(3)
SM-3(1)
MA-3(1)
UGAMS 4937(3)
UGAMS 4938(3)
UGAMS 4939(3)
UGAMS 4941(3)
s/n(4)
s/n(4)
UGAMS 4942(3)
SM-5(1)
MA-5(1)
UGAMS 4946(3)
UGAMS 4943(3)
UGAMS 4944(3)
U-96-150(5)
U-96-148(5)
U-96-149(5)
UGAMS 4944(3)
Localities
(A)
Currais Novos/RN
Barcelona/RN(A)
Maravilha/AL
Maravilha/AL
Poço Redondo/SE(B)
Poço Redondo/SE(B)
Poço Redondo/SE(B)
Gararu/SE(B)
Quijingue/BA
Barcelona/RN(A)
Maravilha/AL
Maravilha/AL
Poço Redondo/SE(B)
Cel. João Sá/BA(B)
Canhoba/SE(C)
Cel. João Sá/BA(B)
Ourolândia/BA
Ourolândia/BA
Rui Barbosa/RN(A)
Maravilha/AL
Maravilha/AL
Poço Redondo/SE(B)
Cel. João Sá/BA(B)
Cel. João Sá/BA(B)
Pedra Vermelha/BA
Ourolândia/BA
Ourolândia/BA
Vitória da Conquista/BA(D)
Lat (°S)
δ13C (‰) on st
14
C age ±1σ on st (14C yr BP)
6
6
9
9
9
9
9
10
10
6
9
9
10
10
10
10
10
10
6
9
9
9
10
10
10
10
10
14
0.50 (d)
5.22 (d)
0.30 (d)
−12.00 (d)
−6.65 (d)
−3.85 (d)
−2.45 (d)
−3.25 (d)
−18.20 (b)
0.44 (e)
0.00 (d)
1.47 (d)
0.76 (e)
−1.04 (e)
−1.86 (e)
−0.49 (e)
−8.20 (e)
−5.00 (e)
−1.32 (e)
−4.10 (d)
1.51 (d)
−3.68 (e)
−1.08 (e)
−1.00 (e)
−5.50 (e)
−12.60 (e)
−7.70 (e)
−13.24 (e)
15,490 ± 40
–
–
–
–
22,440 ± 50
–
–
15,770 ± 40
16,150 ± 40
–
–
–
13,980 ± 40
17,910 ± 50
–
–
–
10,730 ± 30
–
–
10,050 ± 30
–
–
–
–
–
10,970 ± 30
(b)
(d)
(b)
(e)
(e)
(e)
(e)
(e)
(e)
Calibrated age⁎ (2σ range, cal yr BP)
18,580–18,850
–
–
–
–
26,690–27,690
–
–
18,730–19,280
18,930–19,450
–
–
–
16,800–17,380
21,180–21,550
–
–
–
12,560–12,720
–
–
11,400–11,750
–
–
–
–
–
12,660–13,050
⁎Calibrated with IntCal98 (Reimer et al., 2009) and calculated with Calib 6.0 (http://calib.qub.ac.uk/calib/calib.html; last accessed 25 September 2012).
(1)
Silva (2009); (2)Drefahl (2010); (3)Our data; (4)Sánchez et al. (2004); (5)MacFadden (2005) Institutions. (A)Museu Câmara Cascudo/Universidade Federal do Rio Grande do Norte;
(B)Laboratório de Paleontologia/Universidade Federal de Sergipe; (C)Memorial de Sergipe/Universidade Tiradentes; (D)Laboratório de Geologia/Universidade Estadual do Sudoeste
da Bahia.
Please cite this article as: Dantas, M.A.T., et al., Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical
Region, Quaternary Research (2012), http://dx.doi.org/10.1016/j.yqres.2012.09.006
M.A.T. Dantas et al. / Quaternary Research xxx (2012) xxx–xxx
Results
Paleoecology
E. laurillardi
δ13C values found in the dentin of the fossil teeth from Sergipe display a variation between −6.65‰ and −2.45‰ (Table 1). This range
indicates that this species probably had a generalist diet, consuming
C3 and C4 plants (MacFadden et al., 1999; MacFadden, 2005). Even
more negative values were found in the specimens collected in Alagoas
(δ 13C = −12.00‰: Silva, 2009) and Bahia (δ 13C = −18.20‰: Drefahl,
2010) states, but they indicate an exclusive diet of C3 plants.
The data collected from E. laurillardi fossils, of the Rio Grande do
Norte state, showed that this species also had a C4 plant diet (δ13C =
0.50‰ and 5.22‰). Similar values were found by Viana et al. (2011)
in fossil material from Alagoas (δ13C = 0.30‰).
Although the dental morphology of this species precludes grazing,
Bargo et al. (2006) observed that Megatherium americanum and probably E. laurillardi as well, presented a high capability of oral processing
and a strong bite. The former feature could suggest a low digestive efficiency and the latter would allow feeding on material ranging from
moderate to soft consistency, similar to what is found in leaves and
some fruits. An omnivore diet for Megatheriines (M. americanum) was
proposed by Fariña (1996), but the hypothesis was never tested.
N. platensis
The specimens from the north of Bahia, Sergipe and Rio Grande do
Norte showed similar values of δ13C in tooth enamel, varying between
−1.86‰ and 0.76‰ (Table 1). Similar values were found in fossil material from Alagoas, in which δ 13C = 0.00‰ and 1.47‰ (Silva, 2009; Viana
et al., 2011), indicating a diet comprised of C4 grasses. However, a generalist diet (C3 and C4 plants; δ 13C = −8.20‰ and −5.00‰) was also
attributed to mastodonts found in the central part of Bahia by Sánchez
et al. (2004). This type of diet was suggested by Guimarães et al.
(2008) as well, and confirmed by Asevedo et al. (2011a,b), who based
their analysis on teeth microwear and tooth calculus obtained from
the fossil material of the Toca do Gordo do Garrincho, Piauí (PI);
Águas do Araxá, Minas Gerais (MG) and São José do Itaboraí, Rio de
Janeiro (RJ).
T. platensis
In the analyses of carbon isotopes for this species, δ13C values ranging from −3.68‰ to −1.00‰ (Table 1) were found in the material from
the north of Bahia, Rio Grande do Norte and Sergipe. Similar values were
obtained by Silva (2009) and Viana et al. (2011) when they worked
with material from Alagoas (δ13C = −4.10‰ to 1.51‰). These values
indicate a diet based on C4 grasses. However, more negative values
were obtained in our analyses of the remains from the south of Bahia
(δ 13C = −13.24‰), similar to the values presented by MacFadden
(2005) for fossil material collected in Ourolândia, northeastern Bahia
(δ 13C = −12.60‰ and −7.70‰) and Pedra Vermelha, in the north of
Bahia state (δ13C = −5.50‰). These results indicate that this species
had a mixed diet as well (C3 and C4 plants).
2010, Table 1). The compilation of these dates reveals that this species
lived in the BIR during the upper Pleistocene, 27–15 ka (Table 2).
The age assigned to the N. platensis samples (Table 1) varied from
16,800–17,380 cal yr BP (13,980 ± 40 14C yr BP, UGAMS 4938) to
21,180–21,550 cal yr BP (17,910 ± 50 14C yr BP, UGAMS 4939). This
is the species for which the largest number of specimens was previously dated (Table 2). Our results confirm the occurrence of this species between 17 ka and 22 ka. When the results of all published dates
are combined, the occurrence of this species is estimated between
71 ka and 10 ka (Table 2).
The ages assigned to the material of T. platensis (Table 1) ranged
between 11,400–11,750 cal yr BP (10,050±30 14C yr BP, UGAMS 4946)
and 12,660–13,050 cal yr BP (10,970±30 14C yr BP, UGAMS 4944).
These ages reinforce the occurrence of this species in the beginning of
the Holocene in the BIR as shown by Ribeiro et al. (in press; Table 2).
These results combined with others from previous dating analyses indicate the occurrence of this species between 50 ka and 9 ka (Dantas et
al., 2011; Ribeiro et al., in press; Table 2).
Discussion
Available chronological data (e.g. Auler et al., 2006; Dantas et al., 2011;
Ribeiro et al., in press) indicated that E. laurillardi, N. platensis and T.
platensis were present in the BIR during a long period of humidity at the
end of the Pleistocene, between 40 ka and 10 ka. During this period the
rainforests expanded (Behling et al., 2000; Auler and Smart, 2001;
Sifeddine et al., 2003; Barreto, 2010), possibly providing a connection between the Atlantic forest and the Amazon rainforest. Although some pollen data for the dry forests (e.g. De Oliveira et al., 1999) and fossil leaves
for the Atlantic forest of the BIR (e.g. Souza-Lima and Farias, 2008) pointed to a Pleistocene age, it is uncertain how these biomes were distributed
in the BIR during the end of the Pleistocene.
Due to this uncertainty, maps of potential distribution of the Atlantic
forest (Carnaval and Moritz, 2008) and of the dry forests (savannah or
steppic savannah; Werneck et al., 2011) comprising a period of 21 ka
(Fig. 1) were used in order to observe the distribution of the studied
fauna in relation to the biomes. We verified that the studied taxa were
present both in open and closed environments.
The resulting 13C data were grouped into three sub-regions: A (Rio
Grande do Norte); B (Alagoas, Sergipe and north of Bahia); and C (south
of Bahia). We considered that these species had the same diet in open
environments, while in closed environments they showed differences,
ranging from mixed feeders to exclusive C3 plants feeders (Table 1; Fig. 2).
With regard to the 13C data, both ANOVA (E. laurillardi, Fobs =16.11,
P=0.0029; N. platensis, Fobs =19.60, P=0.0018; T. platensis, Fobs =
10.77, P=0.0058) and non-parametric Kruskal–Wallis tests (E. laurillardi,
Hobs =7.02, P=0.0298; T. platensis, Hobs =7.09, P=0.0288) indicate
Table 2
Compilation of the geochronological data for the species Eremotherium laurillardi,
Notiomastodon platensis and Toxodon platensis found in fossiliferous deposits
(“tanks” and caves) in the Brazilian Intertropical Region.
Species
Age, ka
10−15 15−20 20−25 25−30 30−35 35−40 40−45 45−50 50−55 55−60 60−65
Radiocarbon dating
The 14C dating analyses were performed using AMS for the
E. laurillardi samples (Table 1) from the municipalities of Poço
Redondo/SE and Currais Novos/RN. The results were, respectively,
26,690–27,690 cal yr BP (22,240 ± 50 14C yr BP, UGAMS 4932) and
18,580–18,850 cal yr BP (15,490 ±40 14C yr BP, UGAMS 4935). The
age assigned for the sample of Sergipe state is the oldest reported for
this species, whereas the age assigned to the material from Rio Grande
do Norte is similar to the age obtained in two previous analyses using
different techniques (Auler et al., 2006, U 238/Th230, 15 ka; Drefahl,
3
(1,2,3)
E. laurillardi
N. platensis
(4)
T. platensis
(3, 8, 9)
(3)
(3)
(3)
(5)
(5,6)
(4)
(8)
(6)
(7)
(6)
(1)
Auler et al. (2006), (2)Drefahl (2010), (3)Our data, (4)Oliveira et al. (2010),
Kinoshita et al. (2005), (6)Dantas et al. (2011), (7)Kinoshita et al. (2008),
(8)
Ribeiro et al. (in press), (9)Neves et al. (2007).
(5)
Please cite this article as: Dantas, M.A.T., et al., Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical
Region, Quaternary Research (2012), http://dx.doi.org/10.1016/j.yqres.2012.09.006
4
M.A.T. Dantas et al. / Quaternary Research xxx (2012) xxx–xxx
both dental microwear analyses and tooth calculus suggested that
N. platensis had the same type of diet, revealing that the same environmental conditions were present at the localities of Toca do Gordo do
Garrincho/PI, Água de Araxá/MG, and São José do Itaboraí/RJ (Fig. 1).
Conclusions
Figure 2. Tooth enamel carbon isotope (13C) values for the species analyzed in this study.
statistically significant differences among the three geographic samples.
The only exception was the Kruskal–Wallis tests for N. platensis which
indicated the same diet in all sub-regions.
Between the latitudes 6°S to 9°S, there is a wide area (sub-region A,
Fig. 1) in which the dry forests seemed to be predominant, most probably Caatinga vegetation (Behling et al., 2000; Werneck et al., 2011).
The material concerning the three species which were collected in Rio
Grande do Norte gives δ13C values that indicate a diet based exclusively
on C4 grasses (Table 1). It is possible that in this kind of environment
these species had a high competition for resources since they shared
similar niches.
South of latitude 9°S, in the region of Alagoas, Sergipe and northern
of Bahia (sub-region B, Fig. 1), N. platensis had the same diet based
exclusively on C4 grasses, which indicates that this was perhaps its predominant diet (Table 1), while E. laurillardi and T. platensis stopped
feeding exclusively on C4 grasses and start browsing on C3 plants, thus
becoming generalists (Table 1). The exclusive C3 plant-feeder value
found in a sample from Alagoas for E. laurillardi (δ13C = −12.00‰,
Silva, 2009) can be explained as a migrant specimen which came from
Bahia. We infer that these C3 values are not from grasses, because a similar isotopic signal of C3 grass and browse plants occurs only at high latitudes (>35°S) or at high elevations (>3000 m) (MacFadden, 2005),
which are not characteristic of our area of study. The vegetation in
this region (sub-region B, Fig. 1) during this period is interpreted as a
mosaic of dry forests (steppic savannah) and rainforests (Atlantic
forest), where the species could occupy different niches and consequently reduce the competition for resources.
In most of Bahia state (except for the northern region), and perhaps
Minas Gerais, Piauí and Rio de Janeiro states, there would be the predominance of the Atlantic forest (Sub-region C, Fig. 1; Carnaval and
Moritz, 2008), comprising a more closed area than found between latitudes 6°S and 10°S. Drefahl (2010) presented 13C data concerning
E. laurillardi (Table 1) in this region, suggesting that in closed environments the diet of this species consisted exclusively in C3 plants. The
fruits would be one of its main sources of food, thus the taxon is pointed
as one of the main dispersal vectors of different botanic species
(Guimarães et al., 2008). The data available for T. platensis and
N. platensis pointed that in more closed environments these species
fed more in C3 brows plant than in C4 grasses, tending to be exclusive
C3 plant feeder (Table 1).
Other evidence also supports this hypothesis. For example, the 13C
data indicate the same type of diet for the fossil material related to
these species. The material was found in a forest environment of the
Amazon basin and its age ranged from 38.5 to 15 ka (Rossetti et al.,
2004; MacFadden, 2005). Besides, Asevedo et al. (2011a,b) through
The fauna composed of the populations of E. laurillardi, N. platensis and
T. platensis shows different diets throughout the Brazilian Intertropical
Region, varying from exclusively grass feeders to mixed feeders. Thus,
this fauna should not be used as an indicator of open environments, as
Rossetti et al. (2004) previously stated.
In a more closed environment these species tended to feed more on
C3 plants, while in open area environments these species fed on C4
plants. In the latter, these species probably had a major competition
for resources, which led them to have a population below its ideal number. Based on the carbon isotopic analysis, we considered that the ideal
habitat for these species to be a mixed environment of Atlantic and dry
tropical forest, since they presented different kinds of diet, which
should decrease the competition for resources, and, maybe, allowed
them to reach the ideal number of individuals for its populations.
Acknowledgment
We thank CAPES for the doutorament (doctoral) scholarship given to
the first author, and FAPEMIG and USFISH for resources that helped with
fields and the analysis. We thank Priscila Torres and Ale Boss for the
English review of the manuscript, Adriana Bocchiglieri for the help in
the statistical analyses, and anonymous reviewers whose corrections
and suggestions improved the quality of this manuscript.
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Please cite this article as: Dantas, M.A.T., et al., Paleoecology and radiocarbon dating of the Pleistocene megafauna of the Brazilian Intertropical
Region, Quaternary Research (2012), http://dx.doi.org/10.1016/j.yqres.2012.09.006
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Paleoecology and radiocarbon dating of the Pleistocene megafauna