Quaternary Science Reviews 32 (2012) 75e85

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Quaternary Science Reviews

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Unravelling the Late Pleistocene habitat of the southernmost woolly mammoths

in Europe
A. García-Alix a, *, A. Delgado Huertas a, E. Martín Suárez b
a
Instituto Andaluz de Ciencias de la Tierra (IACT-CSIC-UGR), Consejo Superior de Investigaciones Científicas Universidad de Granada, Avenida de las Palmeras n
4,
18100 Granada, Spain
b
Departamento de Estratigrafía y Paleontología, Universidad de Granada, 18071 Granada, Spain

a r t i c l e i n f o a b s t r a c t

Article history: The southernmost record of woolly mammoths (Mammuthus primigenius) in Europe has been found in
Received 5 July 2011 Late Pleistocene sediments from ‘El Padul’ peat-bog, in the Granada Basin (southern Spain). In this paper
Received in revised form we discuss a plausible habitat based on stable isotopic analyses of these specimens, dated w40e30 cal ky
4 November 2011
BP, probably corresponding with the beginning of Heinrich Stadial 4 (HS4) and the end of Heinrich
Accepted 8 November 2011
Available online 29 November 2011
Stadial 3 (HS3). Woolly mammoth remains preserve an accurate isotopic register of past climatic
conditions because they needed to ingest large amount of resources daily (water and fresh food), whose
isotopic signature, influenced by the environmental conditions, was recorded in their tissues. The d18Ow
Keywords:
Stable isotopes
values of the past meteoric waters (5.4& to 6.7& vs V-SMOW), calculated from the isotopic
Woolly mammoth composition of teeth enamel, suggest moderate temperatures in comparison with those of similar age
Latest Pleistocene recovered in central and northern Europe. Due to its geographic position in southern Europe, our
‘El Padul’ peat-bog samples recorded the highest d18Ow values of past meteoric waters deduced from mammoth remains in
Granada Basin Europe. The difference between these values and those of d18Ow of current mean annual precipitation are
minimal, contrasting with those of higher latitudes during the end of the last glaciation (w50 to w20 cal
ky BP). The isotopic values of nitrogen (10.1& to 13.2& vs AIR) and carbon (20.7 to 21.8& vs V-PDB) of
collagen show a dry habitat, which occasionally could have been extreme. Taken as a whole, the isotopic
results suggest that the studied specimens lived in a very dry steppic area, with moderately cold
conditions, contrasting with the wet environment of ‘El Padul’ peat-bog, and its colder temperatures, due
to the influence of glacial conditions of the Sierra Nevada, the highest peninsular mountain range. The
described habitat may be sited in a more westerly position than the ‘El Padul’ peat-bog, and it was
warmer and drier than those of contemporaneous European woolly mammoths.
Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction latest Pleistocene/Holocene boundary, although some isolated

The ‘El Padul’ peat-bog, located in southern Iberia (Fig. 1), has
yielded exceptionally well preserved remains of Mammuthus
primigenius (woolly mammoth) from the Late Pleistocene. It
constitutes the southernmost record of the species in Europe
(Aguirre et al., 1973; Álvarez-Lao et al., 2009). Its presence in this
southern latitude has important paleobiogeographical and paleo-
climatic implications, because the distribution of this taxon is
highly controlled by the existence of cold and dry environments
(mammoth steppe) (Guthire, 1982). M. primigenius appeared in
Europe around 200 ka BP, extending from Siberia, where older
records are present (Lister et al., 2005), and it disappeared in the
* Corresponding author.
E-mail address: agalix@ugr.es (A. García-Alix).
populations survived until w4.0 cal ky BP (Stuart, 2005).
Large mammals, especially proboscidean, need huge inputs of
water supply and fresh food, whose isotopic signature is recorded
in their skeletal tissues (Longinelli, 1984; Luz et al., 1984; Luz and
Kolodny, 1985; among others). That isotopic composition is strongly
influenced by environmental factors; therefore, stable isotope
analyses in fossil mammals can be a successful tool for paleoenvir-
onmental and paleoecological reconstructions (Longinelli, 1984; Luz
et al., 1984; Delgado Huertas et al., 1995; Tütken and Vennemann,
2009; among others).
Oxygen isotopic composition of biogenic carbonates and phos-
phates of mammal bones and teeth depends mainly on the oxygen
signature of the ingested water, due to their constant body
temperature (w37
C) (Longinelli, 1984; Luz et al., 1984; Iacumin
et al., 1996); thus, it has been employed for assessing past
hydrological conditions (D’Angela and Longinelli, 1993; Bryant

0277-3791/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.quascirev.2011.11.007
76 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85
4º00’
10 km
GRANADA
BASIN
Sierra
37º00’
37º00’
Nevada
Granada
Padul area
Neogene and Quaternary
Betic
External Zones and flysch units
Cordillera
Internal Zones
4º00’
Fig. 1. Geographic and geologic location of ‘El Padul’ peat-bog.
et al., 1996; Delgado Huertas et al., 1997; Tütken and Vennemann,
2009; among others). The isotopic composition of collagen
(DeNiro and Epstein, 1978, 1981; DeNiro 1985; Ambrose, 1990;
Bocherens et al., 1991; among others), complemented by the
isotopic composition of carbonates (Iacumin et al., 1997; Koch, 2007;
among others), has been used in order to estimate paleodiets.
This paper tries to unravel the environmental conditions
existing when woolly mammoths colonized the southern areas of
the Iberian Peninsula during the latest Pleistocene. We propose
a multi-isotopic approach by mean of stable isotopes, carrying
out analysis in collagen, carbonate and phosphate (O, C, N) of
mammoth teeth and bones.
2. Regional setting
The ‘El Padul’ peat-bog is located about twenty kilometres south
of the city of Granada, near the village of El Padul, in the western
edge of Sierra Nevada Mountain Range (Fig. 1). It is a subsident
continental sub-basin in the south-eastern sector of the Granada
Basin (Nestares and Torres, 1998; Viseras et al., 2001). It is an
asymmetric graben limited by two-fault systems, one in the
northeastern side, and other in the southwestern side (Delgado
et al., 2002), which constitutes an endorheic depression near of El
Padul village (Nestares and Torres, 1998; Ortiz et al., 2004). Its
infilling is comprised mainly of peat deposits and sediments
(gravels, sands and lutites), eroded from the surrounding triassic
alpujarid basement, ranging from Early Pleistocene to Holocene
(Ortiz et al., 2004). Nowadays the main hydrological supply
proceeds from infiltration of the adjacent reliefs, as in the last
400 ky (Ortiz et al., 2004, 2010).
The studied remains are sited in the upper w10 m of the
sequence, consisting mainly of peat, and proceed from a level of
a peat-bog quarry. Radiocarbon dates from fossil remains, cali-
brated with Calpal program (Weninger et al., 2007), were taken
from Álvarez-Lao et al. (2009). Remains from this level have been
dated in: w40.4  1.2 cal ky BP (carpal bone), w38.7  1.8 cal ky BP
(mandible a) and w30.6  0.7 cal ky BP (mandible b); however in
other sectors of the peat-bog, mammoth remains have been found
with intermediate age (w33.6  0.8 cal ky BP) (Álvarez-Lao et al.,
2009). The 14C method is used to date samples with ages up to
w50 ky BP, but the uncertainty of the measurement increases in
older samples (Weninger, 1986; Weninger and Jöris, 2004); there-
fore, the oldest specimens from the same studied level could have
a similar age, around 40e39 cal ky BP. The youngest mandible
(30.6  0.7 cal ky BP) was located on the top of the level. According
to Álvarez Lao (2007), all specimens from the studied level are
adults, having a minimum age around 43e45 African Elephant
Years (AEY) from Laws (1966). Other remains have been obtained
from the same level, however we were not able to analyze them
because they are badly preserved and/or treated with consolidants.
3. Methodology
There is a degree of variability between the isotopic signatures
of teeth (dentine and enamel) and bones (Bocherens et al., 1992,
1996; Fizet et al., 1995; among others). Mammal bones growth by
apposition of new bone tissues and reabsorption/remodeling/
reconstruction of previous ones, which imply substantial mobili-
zation of mineral compounds; these growing processes slow down
in adult age (Castanet and Ricqlès, 1987; Klevezal, 1996). The
development of remodeling processes and Harvesian systems
(secondary osteones) is very extensive in large mammals (Khöler
and Moya-Sola, 2009). Teeth usually do not register remodeling
processes, and their composition remains unalterable from its
eruption, through the animal’s life (Balasse et al., 1999). Thus,
isotopic composition between a tooth section and bones of the
same specimen may differ because the first one is correlated with
metabolic and environmental conditions of a specific moment
when it forms, and the second one usually shows the mean isotopic
composition (average of the metabolic and environmental condi-
tions) of that bone during the life (or a long period of time) of the
mammal. This fact is specially significant in taxons without
continuous tooth growth, because most of the teeth erupt in
childhood and their isotopic composition may be affected by
weaning (Bocherens et al., 1996; Lindars et al., 2001); however, in
species with continuous tooth growth (teeth that continue growing
through the life of the animal) they record different isotopic
signatures from the top of the crown to the root, and since they
usually do not register remodelling process, they allow us to
reconstruct the environmental variations throughout a period in
the mammal’s life (Bocherens et al., 1994, 1996; Lindars et al., 2001).
In our case, proboscideans generate different enamel lamellae
through their lives, so we can gather environmental data from
distinct time periods during the specimen’s lifespan (Hoppe and
Koch, 2006; Arppe, 2009).
Samples were collected from an excavation in a quarry at ‘El
Padul’ peat-bog during 1983, and nowadays they are exhibited at
the “Parque de las Ciencias de Granada” and at the Museum of the
Department of “Estratigrafía y Paleontología” of the University of
Granada. Seventeen samples, physically cleaned, have been taken
in two molars and one carpal bone.
The studied teeth are: an isolated upper third molar (M3) and
the posterior part of a lower second molar (m2; one lamella in front
of the anterior border of the m3) from a mandible dated with 14C
(30.6  0.7 cal ky BP; Álvarez-Lao et al., 2009). The M3 was well
preserved, and we have sampled three points near of the occlusal
surface: one in the posterior sector, one in the middle, and one in
the anterior sector, trying to pick up enamel (E1, E2, E3), dentine
(D2, D3) and cementum (C2, C3) from each sector. The enamel of
the m2 was well preserved, however, dentine and cementum were
slightly damaged; therefore, we have sampled enamel (E4, E5, E6)
in three points close to the same vertical axis with an approximate
separation of 1.5 cm; cementum (C4, C5, C6) and dentine (D4, D5)
were collected from the single points where they appeared unal-
tered. Lower indexes indicate younger samples. In both molars,
samples were chunks of w1.5 cm in the direction of enamel
growth, which represents approximately one year in the lifespan of
the mammoth, according to Hoppe and Koch (2006) and Arppe
(2009). Therefore, our samples from m2 record time intervals of
one year, and the separations between them represent also about one
 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85 77

year. Samples from M3 record time intervals about one year as well, Table 1
and the separations between them could represent w8e9 years. Isotopic composition of the inorganic fraction of the studied samples. E, enamel; D,
dentine; C, cementum. Lower indexes indicate younger samples (1, 2 and 3: M3; 4, 5
A whole carpal bone was ground and sampled for dating with and 6: M2). d18Oc: oxygen isotopic composition of carbonate (&); d18Op: oxygen
radiocarbon (40.4  1.2 cal ky BP; Álvarez Lao, 2007; Álvarez-Lao isotopic composition of phosphate (&); d13Cc: carbon isotopic composition of
et al., 2009) and for isotopic analyses. carbonates (&); d18Ow: oxygen isotopic composition of meteoric water (&)
We have analyzed carbonate and phosphate from dentine, according to Ayliffe et al. (1992); d18Ow-sw: oxygen isotopic composition of meteoric
water (&) taking into account the isotopic composition of seawater during the end
enamel and cementun of molars. Since the collagen yield from
of last glacial stage (see ‘Discussion, section 5.2’).
cementum and dentine was very poor in our samples, it was
analyzed from a carpal bone and from the dentine-enamel boundary. Specimen Sample d18Oc d18Op d13Cc d18Ow d18Ow-sw
V-SMOW V-SMOW V-PDB V-SMOW V-SMOW
According to Deshpande et al. (2010), the dentine-enamel boundary
contains collagen bundles; so we have sampled the dentine-enamel M3 E1 26.4 17.4 8.2 6.3 7.3
E2 26.3 18.2 10.8 5.4 6.4
boundary (DEB2) from an enamel chunk (E2), because it was the E3 26.1 17.9 7.9 5.8 6.8
only sector of the studied teeth suitable for collagen extraction. D2 26.9 18.3 9.6
Oxygen was analyzed in phosphates and carbonates, carbon was D3 26.4 18.0 7.0
analyzed in carbonates and collagen, and nitrogen was analyzed in C2 26.8 18.2 9.3
C3 26.8 18.2 10.0
collagen.
Oxygen of phosphates was extracted and precipitated as Ag3PO4 m2 E4 25.8 17.0 8.3 6.7 7.7
following the method from O’Neil et al. (1994), slightly modified E5 25.5 17.5 9.7 6.2 7.2
E6 26.3 17.3 9.2 6.4 7.4
(Dettmann et al., 2001; Tütken et al., 2006) by mean of pyrolysis D4 26.2 18.2 6.0
(TC/EA) (Vennemann et al., 2002). Afterwards, phosphates were D5 25.5 18.0 6.4
put into a silver capsule, and introduced into a Thermo Finnigan TC/ C4 25.7 8.9
EA. Pyrolysis released CO at 1450
C, and it was analyzed in C5 25.9 17.6 10.0
C6 26.0 9.6
a Thermo Finnigan XL Mass Spectrometer. Results are expressed in
d notation, using the standard V-SMOW for oxygen. Samples and
standards were measured in triplicate. composition of carbonates (d13Cc). Table 2 shows the carbon and
Oxygen and carbon of carbonates were analyzed using the classic nitrogen isotopic composition of collagen (d13Ccoll and d15Ncoll,
method from McCrea (1950), with some modifications proposed by respectively).
Koch et al. (1997) in order to minimize the effect of the organic The values of d18Op range from 17.0& to 18.3& (V-SMOW),
matter and secondary carbonates. Two milligrams of pre-treated representing a depletion from 7.6& to 9.0& with respect to the
sample was reacted in 100% phosphoric acid at 50
C for 12 h, and d18Oc data of the same samples. d18Oc was analyzed in order to test
the released CO2 was analyzed in a Thermo Finnigan XL mass the preservation of the samples, therefore, we will use only d18Op
spectrometer with a coupled Thermo Finnigan Gas Bench II. Results values for paleohydrological interpretation.
are expressed in d notation, relative to the standard V-PDB (carbon) The results of d13Cc range from 10.8& to 6.0& (V-PDB), and the
and V-SMOW (oxygen). Samples were measured in triplicate. higher values (>7&) correspond to those of dentine, except for the
Collagen was extracted according to the method from Bocherens sample D2, whose value is 9.6. Cementum values range
et al. (1991, 1997). Samples were introduced in tin capsules and from 10.0& to 8.9&, and enamel from 10.8& to 7.9& (V-PDB).
analyzed in a Thermo Finnigan XL mass spectrometer with Isotopic values of bone collagen are: d13Ccoll 21.8& (V-PDB)
a coupled Elemental Analyzer (EA). Results are expressed in and d15Ncoll 10.1& (AIR). Isotopic values of DEB2 collagen are:
d notation, using the standard V-PDB (carbon) and AIR standard d13Ccoll 20.7& (V-PDB) and d15Ncoll 13.2& (AIR).
(nitrogen). Samples were measured in duplicate. Following Genoni et al. (1998), Arppe and Karhu (2006), Ukkonen
The calculated precision, after correction for mass spectrometer et al. (2007), Tütken et al. (2007), and Arppe and Karhu (2010), among
daily drift, using standards systematically interspersed in analytical others, it has been used the equation of Ayliffe et al. (1992) in order to
batches, was better than 0.1& for d15N and d13C, and 0.2& for obtain the oxygen isotopic composition of past meteoric waters
d18O in phosphates and carbonates. (d18Ow) from d18Op record of enamel (Table 1). Our data range
Photographs were made with the FEI ESEM QUANTA 400 of the from 6.7& to 5.4& (V-SMOW). Enamel samples represent annual
‘Centro Instrumentación Científica’ of the University of Granada by periods, so the d18Ow values represent the mean annual isotopic
mean of LFD (large field detector) and SSD (solid state detector) composition of the water that the specimen ingested.
detectors. Samples were observed in low vacuum mode (0.5 torr)
without coating, which allows us to analyze the isotopic compo-
5. Discussion
sition of the same samples. The qualitative chemical composition of
the mineral coating was gathered by mean of EDS (Energy
5.1. Preservation of the samples
Dispersive X-ray Spectroscopy) at 20 kV in low vacuum mode.
Samples show a dark crust covering part of their external
4. Results
surface, and inside of dentine fractures. ESEM and EDS analyses

The isotopic data from different mammoth teeth record the Table 2
dietary habits and environmental conditions during variable time- Isotopic composition of the organic fraction of the studied samples. DEB, dentine-
intervals within organisms’ lifespan. The first tooth studied here enamel boundary. d13Ccoll: carbon isotopic composition of collagen (&); d15Ncoll:
nitrogen isotopic composition of collagen (&); %Ccoll: percentage of organic carbon
(M3), contains the record of the last w16e18 years of the organ-
yielded in weight from collagen (%); %Ncoll: percentage of organic nitrogen yielded in
ism’s life, whereas the second one, represented by a mandible with weight from collagen (%); C/Ncoll: atomic C/N ratio from collagen.
one m3 and a posterior lamella of the m2, records about 5 years
interval when the individual was w25e30 years old (following Specimen Sample d13Ccoll d15Ncoll %Ccoll %Ncoll C/Ncoll
V-PDB N-AIR
Laws, 1966).
M3 DEB2 20.7 13.2 35.6 12.7 3.3
Table 1 summarizes the oxygen isotopic composition of phos-
Carpal bone Carpal 21.8 10.1 35.6 12.3 3.4
phate (d18Op) and carbonates (d18Oc), and the carbon isotopic
78 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85

of that coating show high amount of Fe and S, belonging mainly
to pyrite (FeS2), and barite (with strontium) (Fig. 2); some
gypsums have been detected as well. It is usual to find fram-
boidal pyrite (Fig. 2AeE). Cementum and enamel have lower
concentrations of these minerals than dentine. Those coatings
with pyrite, framboidal pyrite and barite are not rare in our
remains, because the sedimentary environment where they
were deposited was optimum to precipitate these minerals:
a peat-bog with anoxic-reducing conditions; this environment
contributed to the preservation of the remains up to now. The
presence of high amount of strontium in barite (Fig. 2F) is due
to the existence of large outcrops of celestine (SrSO4) in Mon-
tevives-Escúzar sector, about 15 km north-westward of ‘El Padul’
peat-bog, which seems to have a huge influence in the past
hydrology of the area. Arppe and Karhu (2006) suggested that
high concentrations of Fe or Mn do not represent a dramatic
alteration of enamel. All these crusts were removed before
sampling.

Fig. 2. ESEM images of the coating that covers some areas of the teeth (AeE): A, cross section of a crust with pyrite and fromboidal pyrite; B, dentine surface (dark), partially covered
by pyrite, framboidal pyrite (grey) and fibrous barite (white); C, dentine surface (dark), partially covered by pyrite and framboidal pyrite (grey); D, detail of framboidal pyrite;
E, detail of fibrous barite partially covered by pyrite. Qualitative chemical composition of barite, obtained by mean of EDS (F).
 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85
According to Williams and Elliot (1989) dentine, cementum and
bone have higher organic composition than enamel. Their inor-
ganic phase can be altered more easily than that of enamel.
Therefore, the oxygen isotopic composition of the inorganic phase
of enamel will be used in our paleoenvironmental interpretations
(following Hillson, 1986; Lee-Thorp and van der Merwe 1987, 1991;
Lee-Throp et al., 1989; Quade et al., 1992; Thackeray and Lee-Thorp,
1992; Ayliffe et al., 1994; among others), more specifically, phos-
phate fraction, because the oxygen isotopic composition of struc-
tural carbonates can be altered more easily (Ayliffe et al., 1992,
1994; Iacumin et al., 1996 among others). However, we have
obtained data of the inorganic composition from dentine and
cementum in order to assess the degree of preservation of the
studied sections.
Values of d18O of mammal bones and teeth (d18Op and d18Oc) are
directly related to those of d18O body water, and therefore, to those
of drinking water (Longinelli, 1984; Luz et al., 1984; Iacumin et al.,
1996; Bryant et al., 1996). To find isotopically altered remains of
mammal bones and teeth showing a good correlation between
d18Op and d18Oc values is improbable because they precipitate in
isotopic equilibrium with the oxygen isotopic composition of body
waters (Iacumin et al., 1996), and the mechanisms of alteration
between both are different (Iacumin et al., 1996; Zazzo et al., 2004).
Therefore it is possible to use these values as a proxy to identify
isotopically altered samples (Iacumin, et al., 1996; Arppe and Karhu,
2006; Tütken et al., 2007; among others). The offset between d18Op
and d18Oc (Δd18Oc-p) of our samples (without taking into account
the values from dentine D4 and D5) have a mean value of
8.5  0.5& in both teeth, agreeing with the expected range for
unaltered samples (according to Iacumin et al., 1996), except for the
dentine samples D4 and D5 (m2), whose Δd18Oc-p values are 7.6&
and 7.8&, respectively.
M3 is a complete tooth, with very good appearance, and without
large fractures or mineralizations. However, m2 is a posterior
fragment whose dentine is very much fractured and mineralized.
Although the two molars passed through similar diagenetic
processes, dentine of the m2 fragment (with lots of fractures) was
degraded more easily than that from M3; this observation is
corroborated by the values of Δd18Oc-p, showing that dentine
samples of the m2 (D4 and D5) are not in the range of unaltered
samples (according to Iacumin et al., 1996). Enamel is more
70º
δ18Op
65º
60º
55º
50º
45 º
40º
35º
18 16 14 12 10
‰ V-SMOW
Fig. 3. Latitudinal variation of d18Op and d18Ow values in European woolly mammoths ranging from w50 to w20 cal ky BP. Left chart shows variation of d18Op values from mammoth
enamel; right chart shows variation of d18Ow from current precipitation (weighted mean annual isotopic composition) and from woolly mammoths (mean values). Oxygen
precipitation data from Delgado Huertas et al. (1991); Raya (2003); IAEA/WMO (2006). Woolly mammoth data (except those from southern Iberia) from Ayliffe et al. (1992); Genoni
et al. (1998); Arppe and Karhu (2006); Ukkonen et al. (2007); Tütken et al. (2007, 2008); Arppe and Karhu (2010).
79
resistant to diagenetic processes (Ayliffe et al., 1992, 1994; among
others), and as we said above, their results from Δd18Oc-p suggest
good preservation in both m2 and M3. d18Op values of dentine and
cementum in the M3 differ only in 0.3& from those of enamel of
the same point, suggesting very good preservation conditions.
The organic phase of the samples (collagen) has been analyzed
in bone and dentine-enamel boundary. Collagen is not always
unaltered in fossil mammals, but it is usually well preserved in
young samples (Koch, 2007), especially from the Quaternary fossil
record (Bocherens et al., 1997). The preservation of collagen can be
estimated by the atomic C/N ratio, which must range from 2.9 to 3.6
according to DeNiro (1985) and Ambrose (1990), or from 3.1 to 3.5,
a smaller interval according to Klinken (1999). Our data shows an
atomic C/N ratio of 3.3 (DEB2) and 3.4 (carpal bone), agreeing with
the range of unaltered collagen. Percentages of the organic carbon
yielded in weight (35.6% in both) agree with the values of intact
collagen (35%) according to Klinken (1999). Therefore, we can
conclude that our samples contain the original collagen signature.
Lee-Throp et al. (1989) established a mean difference between
d13Cc and d13Ccoll (Dd13Cc-coll) of around 6.8  1.4&, agreeing with
that of Clementz et al. (2009) 7.6  0.5&; however, the mean
Dd13Cc-coll values depends on the species, and that value may be
larger in mammals from cold areas (Iacumin et al., 2010); for
instance, in well preserved mammoths the Dd13Ccoll-c values range
from 6.4& to 10.1& (Iacumin et al., 2000; Arppe and Karhu, 2006).
The Dd13Cc-coll values from our samples DEB2 and E2 (9.9&) are in
that range.
5.2. Oxygen values
The d18Op record from this study and the deduced d18Ow values
(according to the equation of Ayliffe et al., 1992), may be used to
infer hydrological conditions in southern Iberia during cold
episodes within MIS3 (from w40 to w30 cal ky BP), such as the
beginning of Heinrich Stadial 4 (HS4), or the end of Heinrich Stadial
3 (HS3) (e.g., Álvarez-Lao et al., 2009; Álvarez Lao and García, 2010).
Woolly mammoths collected from southern Iberia are the
southernmost specimens found in Europe (Aguirre et al., 1973;
Álvarez-Lao et al., 2009). They record the highest d18Op values
ever reported, and hence, the highest d18Ow values deduced from
European woolly mammoths of comparable age (Figs. 3 and 4). This
18
δ Ow -mammoth
18
δ Ow -current
-6 -8 -10 -12 -14 -16
‰ V-SMOW
80 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85
Fig. 4. Mean distribution of mammoth enamel d18Ow (& V-SMOW) values in Europe
from w50 to w20 cal ky BP. Source data, as in Fig. 3.
finding is expected considering the known overall decline in d18Ow
values of meteoric waters with increasing latitude (Rayleigh frac-
tionation; Craig, 1961; Dansgard, 1964). The difference (Dd18Ocw-w)
between the weighted annual mean d18O values of current
precipitation from IAEA stations near to European mammoths
localities (d18Ocw), and those obtained from woolly mammoths
(d18Ow) that lived during the end of the last glaciation (w50 to w20
ky BP), is minimal (near 0&) in the southern Iberian Peninsula
(w38
N) and possibly, in other comparable low- to mid- latitude
localities (Fig. 3). This oxygen isotopic offset between current and
last glacial waters (Dd18Ocw-w) increases northward, reaching the
highest values in polar regions. However, on a smaller scale,
regional anomalies may disguise this trend (Arppe and Karhu,
2010). The Dd18Ocw-w values vary considerably as a consequence
of other factors besides temperature, known as the continental and
altitude effect in central and northern Europe (Arppe and Karhu,
2010). In fact, the Dd18Ocw-w values at 50
N ranges from 1.3& in
western Germany to 2.2& in southern Poland, whereas in southern
Finland (60
N) is around 2.5&. In an extreme case, the difference
between modern d18Ow values and those recorded in the GRIP ice
core (72
N; Greenland) from w50 to w20 cal ky BP is as much as
5& (Johnsen, 1999).
In general, the isotopic composition of meteoric waters during
the Pleistocene showed lower values in glacial stages than in
interglacial ones, associated with lower and higher temperatures,
respectively (Dansgaard and Tauber, 1969; Dansgaard et al., 1993;
Johnsen et al., 2001; among others). However, other local and
regional factors besides temperature may affect the isotopic
composition of meteoric waters (Dansgard, 1964; Longinelli and
Selmo, 2003; Lee et al., 2007; among others). Our d18O data for
glacial meteoric water may result contradictory, because during
cold events from w40 to w30 cal ky BP, values are normally
expected to be lower than recent values, but the opposite trend is
observed in southern Iberia samples. A plausible hypothesis is that
the oxygen isotopic composition of the seawater was higher in
glacial events than in interglacial ones, and therefore, the oxygen
isotopic composition of the rainwater that came from these masses
at low/middle latitudes, and the resulting meteoric water, was
enriched as well (Dansgaard and Tauber, 1969). Some authors
noticed that the oxygen isotopic composition of the ocean around
w40e30 cal ky BP increases about 1& (Lea et al., 2002; Schrag,
et al., 2002; Elderfield et al., 2010; among others). Following
Delgado Huertas and Reyes (2001), and Arppe and Karhu (2010), we
have made a simulation to minimize the effect of the seawater
isotopic composition around 40e30 cal ky BP in the studied
samples. This should probably be considered when d18O values of
present and past waters are compared. Hence, calculations of
paleotemperatures from water d18O values may be estimated more
efficiently using this type of correction. Table 1 shows our simu-
lated values of meteoric waters corrected by the glacial seawater
18
O-enrichment w40e30 cal ky ago (d18Ow-sw).
Matson and Fox (2010) proposed an Ordinary Least Squared
model relating current mean annual precipitation d18Ow values
(MAd18Ow) and mean annual temperature (MAT) in the Iberian
Peninsula: MAd18Ow ¼ 0.419*MAT þ 11.6. If this model is applied to
our d18Ow-sw data, we obtain mean annual temperatures of 11.3
C
in the samples from M3, and 9.9
C in the samples from m2. These
estimated mean annual temperatures are similar to those observed
today in southern Scandinavian Peninsula and Denmark. However,
these results should be taken with precaution because this
approximation is a simplification, and it does not take into account
other factors that may bias the linear-like relationship between
mean annual precipitation d18O values and mean annual
temperature.
The spatial distributions of d18O values of meteoric precipitation
in the Iberian Peninsula overlap with those from local shallow
groundwater and springs (Plata, 1994). Present day measurements
show that there is a gradient in the oxygen isotopic composition of
meteoric/shallow ground waters in the Iberian Peninsula. That is,
the maximum values of d18O are located in southwestern Iberia, and
they decrease progressively toward the centre and northward of
Iberia (Plata, 1994; Araguás-Araguás and Diaz Teijeiro, 2005; IAEA/
WMO, 2006). This trend can be explained by the fact that Atlantic
air masses that enter into the mainland and experience successive
precipitation events become gradually depleted in 18O values.
However, there are some anomalies in this general model (Araguás-
Araguás and Diaz Teijeiro, 2005), including the effect of the Medi-
terranean Sea in close areas, and the influence of Sierra Nevada
Mountain Range in southern Iberia (altitude effect in recharge,
3400 m). Consequently, d18O values from and meteoric and waters
shallow ground-water around El Padul are lower than expected by
the aforementioned simplified model, and d18O values around 8&
to 10& (meteoric, shallow ground-water and springs) and 7&
(precipitation waters) are recorded in the neighboring areas, such
as the city of Granada or ‘El Padul’ peat-bog (Delgado Huertas et al.,
1991; unpublished data). Currently, and at least during the last
50 ky, the circulation of Atlantic air masses penetrates from the
west in the Iberian Peninsula (Araguás-Araguás and Diaz Teijeiro,
2005; Bout-Roumazeilles et al., 2007), and it could generate
a similar distribution pattern in the oxygen isotopic composition of
precipitation/meteoric and shallow groundwaters, including the
glacial seawater 18O-enrirchment. Therefore, the higher values in
the studied time interval would have been found in the eastern
Mediterranean coast (due to the effect of the close Mediterranean
Sea, as nowadays), and in the western sector of the Iberian Penin-
sula, specially the southwestern sector (due to the 18O depletion in
the inland Atlantic air masses).
The current values of d18Ow of ‘El Padul’ area for meteoric waters
are lower than our result of d18Ow-sw for the studied woolly
mammoth from cold phases, even taking into account the simula-
tion of past seawater conditions described above. However they
should have been lower (or at least similar) than modern values in
the same area, due to the fractionation effect of temperature in
 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85
glacial periods. These high values during the end of the last glaci-
ation would be expected in western areas or Mediterranean coast.
Therefore, we can infer that the studied specimens here did not
imbibe primarily waters from the Granada-Padul area.
5.3. Carbon
The values of d13C from mammal remains provide information
about the organism’s diet (Vogel and van der Merwe, 1977; DeNiro
and Epstein, 1978; Lee-Thorp and van der Merwe, 1987; Cerling
et al., 1997; among others). In our specimens, those values have
been obtained from collagen (organic fraction) and structural
carbonate of hydroxyapatite (inorganic fraction); however their
fractionation rate is different (Cerling et al., 1997; Cerling and
Harris, 1999). Both fractions incorporate carbon from different
dietary components (Koch, 2007). The major source of carbon in
collagen is dietary proteins (Jim et al., 2004; Clementz et al., 2009;
among others), but carbon from structural carbonate is related to
the whole dietary carbon, including carbohydrates, lipids, and
proteins (Krueger and Sullivan, 1984; Ambrose and Norr, 1993;
Tieszen and Fagre, 1993; Jim et al., 2004, 2006; Passey et al.,
2005), so we can estimate the mean diet (Ambrose and Norr,
1993; Tieszen and Fagre, 1993).
The values of d13C in C3 plants range from 22 to 35&, with
usual mean values of around 27&: the limit values represent two
extreme and opposite conditions, and the mean values represent
plants in relatively open conditions without significant moisture
stress (Cerling et al., 1997). Under water stress conditions, such as
drought, plants exhibit the highest carbon isotopic values, which
can reach up to 22& in C3 plants (Farquhar et al., 1982; Cerling
et al., 1997). Taking into account the different fractionation rate
and others factors that could affect to herbivore mammals, it would
correspond to a value of w8& in structural carbonate of
hydroxyapatite and slightly higher than 20& in collagen (Lee-
Throp et al., 1989; Cerling et al., 1997). In general, European
woolly mammoth followed a diet of C3 plants during the latest
Pleistocene glacial stage, and their d13C values usually correspond
to the upper range of C3 plants (Bocherens et al., 1997; Iacumin
et al., 2000; Arppe et al., 2011; among others). Arppe et al. (2011)
propose a southwest e northeast gradient based on the carbon
isotopic composition of carbonates from central and northern
European woolly mammoths, where higher d13Cc values were
found in southwestern areas, implying warmer and drier condi-
tions than those found in northeastern areas.
Our data for collagen from bone and teeth (from to 21.8
to 20.7&) and of biogenic apatite from teeth enamel (from 10.8
to 7.9&) are in the range of a pure C3 biomass, as we would
expect during that time interval in the southern Iberian Peninsula,
and the highest values, close to the uppermost boundary, demon-
strate that there was an important water stress in the vegetation,
likely caused by hard dry conditions. d13C values are more extreme
in teeth remains, because they record a smaller gap of time than
those from bones, which record an average value of the animal’s
life. It could mean that our specimens lived occasionally under
extreme arid conditions.
The comparison between the carbon isotopic composition from
El Padul remains, and that from other Eurasian woolly mammoths
(from w50 to w20 cal ky BP) (Iacumin et al., 2000, 2010; Arppe
et al., 2011; among others), reveals that our record agrees with
the highest values measured in other European samples. Interest-
ingly, specimens studied here tracked the highest d13Cc values
during this time-interval, as expected considering the geographical
location. These d13C values suggest warmer and drier conditions in
southern Iberia than in northeastern Europe (according to Arppe
et al., 2011), and agreeing with the calculated d18Ow data from
81
southern Iberia, which pointed to warmer condition than in
northeastern areas.
The Dd13Cc-coll value in our specimens (9.9&) is within the range
of woolly mammoth, from 6.4& to 10.1& (Iacumin et al., 2000;
Arppe and Karhu, 2006), but far from the mean for herbivores
in general: 6.8  1.4&, (Lee-Throp et al., 1989) and 7.6  0.5%
(Clementz et al., 2009), because Dd13Cc-coll values are usually higher
in mammals from cold areas (Iacumin et al., 2010).
5.4. Nitrogen
The nitrogen isotopic composition of animal tissues is related to
its diet (DeNiro and Epstein, 1981), because their main nitrogen
source is dietary proteins (Hedges et al., 2005). The d15N values in
collagen increase between 2e5& in each trophic level from
primary producers to carnivores (DeNiro and Epstein, 1981). Water
stress caused by drier ground conditions produces 15N-enriched
soils, which in turn, increases the d15N values in plants (Heaton
et al., 1986, Sealy et al., 1987; Ambrose, 1991; Handley et al., 1999;
Schwarcz et al., 1999). Dry conditions additionally causes meta-
bolic changes in the urea excretion rates of animals, which enriched
animal tissues in 15N (Sealy et al., 1987; Schwarcz et al., 1999).
Starvation can also increase the d15N values, due to the turnover
protein re-use (Hobson et al., 1993; Hedges et al., 2005; Koch,
2007). In fact, the increase of d15N values with decreasing precipi-
tation (increasing aridity) is much more important in recent
elephants (Ambrose and DeNiro, 1986; Heaton et al., 1986), than in
others taxons of the same area (Gröcke, 1997; Ambrose, 2000).
Nitrogen isotope values of collagen are usually higher in woolly
mammoths than in others contemporaneous herbivores, reaching
in some cases similar values than those of carnivores (Bocherens
et al., 1994, 1996; Iacumin et al., 2000, 2010). Moreover, within
the group of woolly mammoths there is a spatial variability, and, as
in modern proboscideans, specimens that suffer water stress,
starvation conditions or living in dry habitats, show higher d15Ncoll
values than others from less arid or wetter habitats (Bocherens
et al., 1994; Bocherens, 2003; Szpak et al., 2010; among others).
High values of d15Ncoll in mammoths could imply that they lived in
a dry steppe-tundra environment (Szpak et al., 2010). Published
woolly mammoths d15Ncoll values are usually lower than 13& (e.g.,
Iacumin et al., 2000). There are two values of d15Ncoll from the
studied specimens: carpal bone (10.1&) and EDB2 from teeth
(13.2&). As we said above, the isotopic value from bones show an
average diet of the animal’s life, and the value of one point of the
teeth is an occasional/annual value. The bone d15Ncoll value (10.1&)
is high, implying a drier steppe-tundra environment. Interestingly,
the teeth d15Ncoll value (13.2&) is considerably high, showing an
occasional extreme aridity, which could even have lead to the
starvation of the specimen. Therefore, we propose that the envi-
ronment where the studied woolly mammoths lived was a dry
steppe-tundra, with some occasional moments of extreme aridity.
6. Integration of the isotopic data
The presence of woolly mammoths in the ‘El Padul’ peat-bog
seems to be related with general cold episodes within MIS 3, more
specifically, the oldest mammoth remains (w40e39 cal ky BP) can
be associated with the beginning of Heinrich Stadial 4 (HS4), and the
youngest ones (w31e30 cal ky BP) may be probably correlated with
the end of Heinrich Stadial 3 (HS3) (Álvarez-Lao et al., 2009; Álvarez
Lao and García, 2010), taking into account the chronology of the
Heinrich Stadials proposed by Sánchez Goñi and Harrison (2010).
The Heinrich Stadials were global dry and cold periods, which
reached southern Iberia, according to the record of steppic plants
and alkenones in the Alboran Sea and southern Iberian margin
82 A. García-Alix et al. / Quaternary Science Reviews 32 (2012) 75e85
sediments (Sánchez Goñi et al., 2000; Combourieu Nebout et al.,
2002; Martrat et al., 2004, 2007; Eynaud et al., 2009; Sánchez
Goñi and Harrison, 2010). In Iberia, these cold and dry conditions
were related to the displacement of the polar front to the northern
sector of the Iberian Peninsula and the presence of icebergs up to
37
N in the Iberian margin (Eynaud et al., 2009). Marine records of
alkenones from southern Iberian margin (western Mediterranean
and Atlantic) show sea surface temperatures close to 10e11
C
during cold episodes from w40 to w30 cal ky BP, which contrast
with the current 18
C (Martrat et al., 2004, 2007).
According to Ortiz et al. (2010), wet conditions prevailed locally
in the ‘El Padul’ peat-bog during the last 100 ky, but occasional cold
and dry episodes can be identified, linked to rapid changes in
vegetation (expansion of grass-steppe, and retraction of trees),
consistent with Heinrich Stadials and Younger Dryas. However, the
results of the n-Alkane analyses in the sediments of the peat-bog,
which indicate the most likely source of the organic inputs,
suggest that HS4 and HS3 were locally weaker than YD, HS1 and
HS2 (Ortiz et al., 2010). The d13C values from ‘El Padul’ peat-bog
record values from 29& to 27& in the studied period (Ortiz
et al., 2004, 2010), contrasting with our data of d13C from
mammoth remains, which are close to highest values of C3 plants.
Taking into account the local environmental data from ‘El Padul’
peat-bog during the studied interval (Ortiz et al., 2004, 2010),
contrasting with the studied data of d13Ccoll, d13Cc and d15Ncoll,
which are extremely high (dry steppic conditions), especially those
from teeth, we suggest that specimens inhabited during
a predominant period of their lives a drier area than ‘El Padul’ peat-
bog. Our d18O record also implies that specimens of M. Primigenius
did not live their whole lives at ‘El Padul’ site, because the inferred
values for meteoric waters are higher than those expected in ‘El
Padul’ area during cold periods of the end of the last glaciation, such
as Heinrich Stadials, which should be lower (or at least similar)
than the current 9& by the effect of temperature and Sierra
Nevada Mountain Range.
Álvarez Lao and García (2010) suggested that it is likely that the
presence of woolly mammoth (w40.4 to w30.6 cal ky BP) at the ‘El
Padul’ area was sporadic, and related to cold and extreme drought
periods, instead of an isolated population living continuously
during that long period. This affirmation can be corroborated with
our isotopic data. The plausible oxygen isotopic gradient of mete-
oric waters in cold episodes during the end of the last glacial stage
in the Iberian Peninsula, such as HS4 and HS3, suggests that the
inferred values of d18Ow-sw from the studied samples could be
expected in a western area or in a narrow bar in the Mediterranean
coast. However, as for present day, the higher values, consistent
with our data, would be mainly those located in the western areas.
Nevertheless, if we take into account other factors, such as that the
polar front migrated to the northern Iberian margin during Hein-
rich Stadials, (Eynaud et al., 2009); the isotopic value of d18Ow of
these northern areas could have decreased, so, if woolly mammoths
had lived in this region, more negative oxygen isotopic values
would be expected from their remains. Therefore, the south-
western quadrant of the Iberian Peninsula is the most probable area
where our specimens recorded their isotopic signature. Conse-
quently, we propose that our specimens would have lived in the
southwestern sector of the Peninsula, (perhaps less than 200 km
westward of the Granada Basin), rather than in the southern
Mediterranean coast where no woolly mammoths remains have
been found, in agreement with Álvarez-Lao et al. (2009), who
suggested that the Sierra Nevada Mountain Range (Betic Cordillera)
prevented an advance of woolly mammoths to the Mediterranean
coast. Some populations of mammoths have medium migration
patterns, and they could alter their local movements and move
hundreds of km (<500 or <600) (Hoppe et al., 1999; Hoppe, 2004)
in response to changing regional vegetation patterns or local
climatic stresses (Hoppe and Koch, 2007; Barbieri et al., 2008).
Therefore it is possible that populations of woolly mammoth
migrated from western areas of southern Iberia, when conditions
became extremely dry, to ‘El Padul’ area where humidity conditions
were not so extreme according to the geochemical data from Ortiz
et al. (2004, 2010).
7. Conclusions
Seventeen samples from three specimens of Late Pleistocene
woolly mammoths from southern Iberia have been analyzed to
study the isotopic composition of phosphates, carbonates and
collagen tissues in order to reconstruct the past habitat in which
the specimens lived. The state of preservation of our samples, as
demonstrated from the geochemical, ESEM and EDS analyses,
suggested that the isotopic composition of phosphates and
carbonates of enamel, and collagen of bone and dentine-enamel
boundary, was suitable for paleoenvironmental interpretations.
Our specimens lived in Iberia from w40 to w30 cal ky BP,
coinciding with cold and dry phases, such as HS4 and HS3. They
inhabited a dry steppic area with moderate cold temperatures
(w9e11
C).
The record of d18Ow deduced from d18Op data of ‘El Padul’
remains are not consistent with the expectable meteoric water
values from the ‘El Padul’ area during these cold stages, since in that
case, lower oxygen isotopic values would have been expected due
to the effect of Sierra Nevada Mountain Range. Nitrogen and carbon
isotopes suggest that mammoths lived during most of their life in
a drier area than ‘El Padul’ peat-bog. Our results point that the
habitat of these specimens was a dry steppe in southwestern Iberia
(or at least tens or hundreds of kilometres westwards from the
Granada Basin), and that they occasionally migrated to ‘El Padul’
area running away from extreme arid conditions. The inferred
environmental setting of southern Iberia during this period was
drier and warmer than those of central and northern Europe.
As expected by the geographic location, the studied samples
record the highest values of d18Op, and of d18Ow obtained from
mammoth enamel during the end of the last glaciation (w50 to
w20 cal ky BP) in Europe. The difference between the deduced past
d18Ow values and those of the modern weighted mean annual
precipitation is minimal in southern Spain, and they are increasing
to northward latitudes.
Acknowledgements
This study was supported by the projects “CGL2007-65572-C02-
01/BTE” and “CGL2010-21257-C02-01”, the program “Consolider
Ingenio 2010” (CSD 2006-00041) of the Spanish Ministerio de
Ciencia e Innovación, and the research groups RNM0190 and
RMN309 of the “Junta de Andalucía”. A.G.-A. was also supported by
a Juan de la Cierva contract from the Spanish Ministerio de Ciencia e
Innovación. We thank A. Granados for his help in the stable isotope
laboratory (IACT), I.M. Sánchez-Almazo for taking the photographs
(CEAMA, Granada, Spain), S. Foster for improving the English text,
and Y. Yanes for her helpful comments. Remarks and suggestions by
two anonymous reviewers, and by the Editor, J. Carrión, are kindly
acknowledged.
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