ArticlePDF Available

Paleoecological Implications Inferred from Stable Isotopic Signatures (δ13C, δ15N) in Bone Collagen of Ursus spelaeus ROS.-HEIN



Stable isotopic signatures measured in bone collagen provide with data related to the species diet type. In this paper we compare δ13C and δ15N outcomes in Ursus spelaeus ROS.-HEIN. bone remains from Liñares site and Cova Eirós site (Galicia, NW of the Iberian Peninsula). Some data on fossil Ursus arctos L. and Pleistocene Cervus elaphus L. from Galician caves are also presented, as a first approach to distinguish paleodiets of different species inferred from their isotopic signatures. Once all data have been analyzed with proper statistical tools and since this work was planned in order to reduce variation in stable isotopic signals caused by metabolic causes, we may assume that the observed differences between both studied groups are exclusively due to environmental factors and show a migration of the cave bear population in the Serra do Courel mountains from higher to lower altitudes because of the transition from warm climatic conditions to colder ones.
Cadernos Lab. Xeolóxico de Laxe
Coruña. 1999. Vol. 24, pp. 73-87
PPaalleeooeeccoollooggiiccaall iimmpplliiccaattiioonnss iinnffeerrrreedd
ffrroomm ssttaabbllee iissoottooppiicc ssiiggnnaattuurreess
((δδ1133CC,δδ1155NN)) iinn bboonnee ccoollllaaggeenn ooff
UUrrssuuss ssppeellaaeeuuss RROOSS..--HHEEIINN..
Implicaciones paleoecológicas inferidas de la
caracterización isotópica (δ13C,δ15N) del
colágeno óseo de Ursus spelaeus ROS.-HEIN.
Stable isotopic signatures measured in bone collagen provide with data related to the species
diet type. In this paper we compare δ13C and δ15N outcomes in Ursus spelaeus ROS.-HEIN. bone
remains from Liñares site and Cova Eirós site (Galicia, NW of the Iberian Peninsula). Some
data on fossil Ursus arctos L. and Pleistocene Cervus elaphus L. from Galician caves are also pre-
sented, as a first approach to distinguish paleodiets of different species inferred from their iso-
topic signatures. Once all data have been analyzed with proper statistical tools and since this
work was planned in order to reduce variation in stable isotopic signals caused by metabolic
causes, we may assume that the observed differences between both studied groups are exclusi-
vely due to environmental factors and show a migration of the cave bear population in the Serra
do Courel mountains from higher to lower altitudes because of the transition from warm clima-
tic conditions to colder ones.
KKeeyy wwoorrddss: δ13C, δ15N, collagen, paleodiets, Ursus spelaeus, Ursus arctos, Cervus elaphus, paleocli-
matology, Late Pleistocene, Galicia, NW Spain.
Instituto Universitario de Xeoloxía “Isidro Parga Pondal”. Universidade da Coruña. Facultade de Ciencias.
Campus da Zapateira s/n. 15071. A Coruña. Galicia. Spain.
This work goes on with isotopic bio-
chemistry research on Quaternary fossils
from Galician sites, started
(FERNÁNDEZ, 1998) with Ursus spelaeus
ROS.-HEIN. from Cova Eirós. In this
paper we show first outcomes on U. spela-
eus from Liñares site and even some data
from Cervus elaphus L. and Ursus arctos L.
We are going to tackle the reconstruction
of paleoenvironmental changes inferred
from isotopic data got from fossil bone
remains. This kind of studies -recently
started (FERNÁNDEZ, 1998) on
Galician sites- have proved to be a proper
tool in helping the reconstruction of
ancient environments when those are cou-
pled with the most common geological
data, as sediments or geomorphology
(GRANDAL et al., 1997). In the last
years, the knowledge about Quaternary
Period in Galicia (VIDAL ROMANÍ,
1996) has undergone a strong impulse due
to a multidisciplinary approach and the
use of highly specialized techniques,
which contribute to solve the problem of
understanding a period of time so scarce
in fossil data as happens in Galicia.
The objetive of this work is to deter-
mine what kind of paleoenvironmental
conditions surrounded the occupation of
sites such as Liñares and Eirós (GRAN-
DAL, 1998) with an important record of
Pleistocene macrofauna. Both are conside-
red as different steps in the migration pro-
cess of populations happened during gla-
cial terms.
Isotopic signals are thought as impor-
tant tools in order to supporte the hypote-
sis of paleoclimatic changes in late
Pleistocene in Galicia. Such a theory has
been proposed from geological data rela-
ted to glaciar phenomena (VIDAL
ROMANÍ, 1996), faunistic assemblages
found in different sites (GRANDAL et al.,
1997) and some modern techniques for
dating rock surfaces (FERNÁNDEZ,
The meaning of stable isotopic signa-
tures preserved in fossil animal tissues can
vary depending on metabolic or environ-
mental causes. Our attention will be focu-
sed in the cave bear, extinct aproximately
15,000 years ago and with a well known
trend towards herviborism (KURTÉN,
1976). Then, the aim of this paper will be
to analyse isotopic signals of Ursus spelaeus
bone collagen in order to distinguish
whether a qualitative climatic change
existed or not between the ages when
those sites were occupied; taking into
account the influence of climate in the iso-
topic fractionation along the trophic
As stable isotopic outcomes from car-
bon and nitrogen signals in fossil bones
have been used as paleoenvironmental
markers, it should be possible to compare
outcomes with close and distant contem-
poraneous individuals data.
Often, teeth and bones are the only
remains that survive in the fossil record,
but as they are not closed systems, they
can suffer weathering, infiltration and
quite enough damage because of several
process after death; so, a critic step in any
study will be to evaluate collagen preser-
vation. Thus, a suitable C/N atomic value
(between 2,9 and 3,6 after DE
NIRO,1985) will be required. During
74 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 75
diagenesis, C/N values can raise due to
deamination of aminoacids or invasion by
soil humic acids, and even fall because of
inorganic material contamination (TUR-
proving that isotopic signals are original,
and taking into account that collagen
damage is not dependant on time, but fos-
sil preservation conditions (TUROSS &
STATHOPLOS, 1993), isotopic data will
be able to be used as markers of paleoenvi-
ronmental conditions.
Stable isotopic compositions of food
and drinks of animals have a strong
influence on the isotopic compositions of
the tissues they synthesize. Conversely, the
isotopic composition of animals tissues
can serve as a natural tracer of different
dietary inputs with distinct isotopic sig-
natures (DE NIRO, 1985). However, the
exact relationship between the isotopic
compositions of ingested materials and
those associated to any particular tissue or
molecular component is quite complex,
responding not only to changes in nutri-
tional status, but turnover rate of the tis-
sue and biosynthethic pathway. Then, sta-
ble isotope analysis provides more than
just a tracer of the materials that go into
an animal, but it offers a view of the bio-
logical processes within an organism
(KOCH et al., 1994) and thus, some clues
to reconstruct the environment where it
As many authors have noted, the ato-
mic ratio between heavy isotopes and
lighter ones (Rx= mX/nX, being m>n) is
compared with a reference control. Delta
symbol (δ) means the difference between
sample R and the control one (LAJTHA &
MICHENER, 1994). So:
δ(‰) = [(Rsample – R reference)/ R reference].1000
Carbon and nitrogen stable isotope
signatures may differ depending on some
factors. The former element is influenced
not only by isotopic composition of
atmospheric CO2influences, but also by
photosynthesis type (C3or C4) in the base-
ment of trophic chain too. Thus, plants
with Calvin cycle (C3) absorb less 13C from
CO2than Hatch-Slack (C4) ones. Then,
alimentary chains based in a vegetal step
with C3as dominants will be depleted in
the heavy isotope, which -according to
logical fractionations at the same time we
get higher levels- make animal tissues to
have minor δ13C values. We should remark
that C3plants are associated with tempe-
rate or boreal climates, excluding tropical
conditions which are supposed for C4ele-
ments. Moreover, other factors as species,
physiology -example of lipidic catabolism
in ursids during hibernation (ANDER-
SON, 1992)- and kind of tissue might
affect these values (AMBROSE & DE
NIRO, 1989; BOCHERENS et al.,
1991a; KOCH et al., 1994; LAJTHA &
MARSHALL, 1994).
Dealing with nitrogen signal, inputs of
heavy isotope are determined by atmosphe-
ric N2fixation by micoorganisms in sym-
biosis with some particular plant species.
Thus, fixator plants display a lower δ15N
than non-fixators. Several factors affect frac-
tionation process and enrichment when
considering higher trophic steps in the ali-
mentary chain: soil conditionants as humi-
dity, acidity and age, animal physiology,
specific metabolism pathways for nitrogen,
kind of tissue, suckling in mammals and,
only in high vegetal density forest, the
canopy effect (AMBROSE, 1991; BOCHE-
RENS et al, 1991a; BOCHERENS et al.,
1991b; NELSON et al., 1975; CORMIE &
SCHWARCZ, 1994).
SSaammppllee aanndd TTeecchhnniiqquueess
A sample of 38 bone remains from
several Galician sites was assembled. It has
been used 23 cave bear (Ursus spelaeus)
ribs, and the vertebra - Lus24- and meta-
pod -Lus25- used on ancient DNA studies
(VILA, 1998); all of them came rom
Liñares site (Galicia, NW of Iberian
Peninsula) Furthermore, a metatarsian -
Lce1- and 6 ribs from deer (Cervus elaphus)
of Liñares site were also added, as well as 8
ribs of Holocene brown bear (Ursus arctos)
from Tarelo and Purruñal sites (Galicia,
NW Iberian Peninsula). All selected
bones belonged to adult individuals.
Liñares site (LÓPEZ, 1996; LÓPEZ et
al., 1997; GRANDAL & LÓPEZ, 1998)
is a small karst cave, located in the Serra do
Courel mountains, at 1,115 m above sea
level (Fig. 1).
76 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
FFiigguurree 11..-- GGeeooggrraapphhiiccaall llooccaattiioonn ooff LLiiññaarreess ssiittee..
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 77
Figure 1 plots the location of Liñares
& LÓPEZ, 1998) and Tarelo site, where an
Ursus arctos skeleton comes from. The age of
the mentioned sites has been inferred from
absolute datings carried out on bone fossil
remains preserved on their sediments. Thus,
Tarelo site occupation is assumed during
Holocene term due to geomorphological
data and a brown bear bone dated -by 14C
method- in 7,460 ± 95 yBP (GRANDAL et
al., 1997). Liñares site is supposed to be acti-
ve around 35-40,000 yBP, this is inferred
from a Cervus elaphus bone dated around
37,000 yBP (LÓPEZ, 1996; GRANDAL et
al., 1997) and age outcomes for
Ursus spelaeus bone remains from
Liñares were 35,000 ± 1,440 yBP
and >38,000 yBP (GRANDAL et
al., 1997; VILA, 1998).
As %N is a first indicator about
collagen preservation, bone powder
(got after sewing and crashing the
bone) was analyzed in a Carlo-Erba
1108 Elemental Analyzer with
analytical reproducibility better
than 0.1%. Once it was rejected
those bones not suitable enough for
isotopic determination due to their
minimum bone %N (IACUMIN et
al., 1997), we followed a common
extraction method for collagen
(BOCHERENS et al, 1997b) based
on some digestions with HCl and
NaOH and filtrations, in order to
remove carbonates, humic contami-
nants and make soluble the extrac-
tion product. Afterwards, this mate-
rial was freezed-dried and analyzed
by SIRMS (Stable Isotopic Ratios
Mass Spectrometry). Collagen isotopic sig-
nals for carbon and nitrogen were measured
in a Finnigan Mat Delta Plus joint to a
Elemental Analyzer Carlo-Erba 1108 with
analytic reproducibility better than 0.1‰
for carbon and 0.2‰ for nitrogen.
Outcomes are referred to international stan-
dars PDB and atmospheric N2.
Taking into account that well preserved
collagen, from isotopic point of view, would
yield an atomic C/N ratio between 2.9 and 3.6
(DE NIRO, 1985) we must reduce the initial
number of 38 bone samples to 30. Proportions
for each site are shown in figure 2, whereas
final outcomes are shown in table 1.
FFiigguurree 22..-- SSaammppllee ssiizzee ooff tthhee ssttuuddiieedd bboonneess ddeeppeennddiinngg oonn ssiittee
((aa)) aanndd ssppeecciieess ((bb)).. FFiinnaall ssaammppllee ssiizze
e iiss rreedduucceedd dduuee
ttoo tthhee 22..99--33..66 ccrriitteerriioonn ffoorr ccoollllaaggeenn pprreesseerrvvaattiioonn ((DDEE
NNIIRROO,, 11998855))..
78 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
SSaammpplleeBBoonneeYYiieelldd%%NN ccooll%%CC ccoollAAttoommiiccδδ1155NN ccoollδδ1133CC ccooll
%% NNmmgg//ggCC//NN ccooll
Lus1 0.79 70.40 5.70 15.60 3.17 3.04 -21.24
Lus2 2.61 70.63 9.12 24.69 3.14 3.49 -21.23
Lus3 2.44 219.14 8.85 23.99 3.14 3.24 -21.14
Lus4 2.26 111.94 9.07 24.42 3.12 3.35 -20.65
Lus6 3.04 78.48 11.80 32.16 3.16 3.35 -20.86
Lus7 2.35 85.12 7.41 20.71 3.24 3.56 -21.50
Lus8 3.09 98.86 10.34 28.40 3.19 3.12 -20.87
Lus9 2.52 88.57 12.10 32.73 3.14 2.93 -20.97
Lus10 2.09 30.87 13.19 35.51 3.12 3.20 -20.90
Lus11 2.67 50.54 11.64 30.74 3.06 2.96 -21.28
Lus12 2.64 112.82 13.45 36.20 3.12 2.81 -20.63
Lus13 0.55 35.45 8.53 17.69 3.07 3.11 -21.41
Lus14 0.59 36.30 7.86 20.45 3.02 2.15 -21.13
Lus16 3.06 92.88 8.80 23.92 3.16 3.18 -20.97
Lus17 2.33 55.08 10.25 27.89 3.16 3.39 -21.72
Lus18 3.02 86.31 9.98 25.77 3.00 2.17 -20.92
Lus19 2.48 73.16 10.83 30.21 3.24 3.61 -20.92
Lus20 3.01 67.43 11.93 31.95 3.11 3.05 -20.77
Lus24 2.68 127.68 7.55 20.49 3.15 2.92 -21.23
Lus25 3.07 229.08 9.07 24.41 3.12 2.11 -20.94
Lce2 2.76 59.06 6.40 17.20 3.12 5.88 -19.65
Lce3 2.69 83.14 12.33 33.15 3.12 7.42 -19.92
Lce4 2.85 56.81 6.64 18.17 3.18 5.71 -20.10
Lce5 1.94 49.09 10.31 27.37 3.08 6.19 -19.72
Lce6 2.98 67.92 10.86 29.17 3.12 6.18 -20.00
Lce7 3.00 59.14 10.53 28.27 3.11 6.65 -19.77
Pua1 3.05 139.39 12.01 32.64 3.15 5.21 -20.00
Pua2 2.62 143.26 13.94 36.95 3.08 5.40 -19.54
Pua3 2.43 111.05 12.79 32.52 2.95 4.94 -19.41
TTaabbllee 11..-- OOuuttccoommeess ffrroomm 3300 bboonnee ssaammpplleess.. LL ((ffiirrsstt lleetttteerr ffrroomm ssiittee aass ffiigguurree 22,, LLiiññaarreess)),, uuss ((iinniittiiaall ooff
ssppeecciieess,, UUrrssuuss ssppeellaaeeuuss))..
According to previous works (BOCHERENS, 1997; CORMIE & SCHWARCZ,
1994), isotopic signals allow to distinguish different species. Following those references
we can ensure that isotopic signals for the Cervus elaphus and Ursus arctos remains inclu-
ded in this paper are feasible. (Fig. 3).
FFiigguurree 33:: IIssoottooppiicc ssiiggnnaattuurreess oouuttccoommeess ffoorr UUrrssuuss
ssppeellaaeeuuss (( )),, CCeerrvvuuss eellaapphhuuss ((³³)) aanndd UUrrssuuss
We have chosen a Kruskal-Wallis test,
which works with sample median instead
of the mean, in order to resolve whether
differences in δ13C are significant. Results
are shown in figure 4.
FFiigguurree 44..-- SSiiggnniiffiiccaanntt ddiiffffeerreenncceess iinn δδ1133CC ddeeppeennddiinngg
oonn ssppeecciieess.. CCaavvee bbeeaarr vvaalluueess aarree rreeaallllyy ddiiffffee--
rreenntt ffrroomm ddeeeerr aanndd bbrroowwnn bbeeaarr oonneess:: pp--
luuee 00..0000001144.. KKrruusskkaall--WWaalllliiss tteesstt rreessuullttss
aaggrreeee wwiitthh AANNOOVVAA--II.. SSeeggmmeennttss sshhooww tthhee
iinntteerrvvaall ((9955%% ccoonnffiiddeen
nccee)) ggoott ffoorr ssaammppllee
mmeeaann ((++)).. NNoottcchh sseettss mmeeddiiaann ppoossiittiioonn..
Another Kruskal-Wallis test proved
that differences for δ15N were significant
depending on species: p-value < 0.05. So,
our 30 data agree with trophic levels for
these species (IACUMIN et al., 1997;
Focusing in Ursus spelaeus isotopic sig-
natures, we should remark the difference
in δ15N depending on age stage
(FERNÁNDEZ, 1998). Data from Eirós
non-suckling individuals will be plotted
in figure 5 together with Liñares cave bear
in order to distinguish differences in
nitrogen signatures
FFiigguurree 55..-- CCaarrbboonn aanndd nniittrrooggeenn ssttaabbllee iissoottooppiicc ssiigg--
nnaallss ooff UUrrssuuss ssppeellaaeeuuss bboonnee ccoollllaaggeenn.. δδ1155NN
iinnddiiccaatteess ttwwoo sseeppaarraattee ggrroouuppss ddeeppeennddiinngg oonn
tthhee ssiittee..
We can appreciate that Liñares data are
close grouped. δ13C variation among indi-
viduals is not higher than ± 0.5 ‰ nor
δ15N one is higher than ± 0.6 ‰ (WANG
& CERLING, 1994). Thus, inside each
population, variation is caused by metabo-
lic parameters, whilst variation among
different populations would be due to
environmental ones.
A t-Student test for δ13C depending on
site, Eirós and Liñares, shows no signifi-
cant differences (p-value < 0.05). A U-
Mann-Whitney for δ15N let us reject (p-
value < 0.0001) the null hypothesis of
similar medians between Eirós and Liñares
data (see figure 5).
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 79
As the extraction product is true colla-
gen, with a C:N ratio close to 3, it can be
seen in figure 6 that the regression line got
from Liñares bones (cave bear and deer)
shows a slope close to the proposed value.
Brown bear remains from Purruñal site fit
properly to this linear trend.
Determination coefficient, R2, also agree
with the hypothesis of collagen as extra-
tion product: 96.07 % of sample variabi-
lity can be explained by a linear regression.
Whereas, the Eirós equation for the
same parameters was:
YY == 22..5522 XX ++ 11..440022; Pearson r= 0.991
(FERNÁNDEZ, 1998).
By testing -with a paired t-test- the
null hypothesis of non difference between
collagen %C mean from Eirós to Liñares,
we got a p-value = 0.57, and we cannot
reject such a null hypothesis. Same fact
was obtained for collagen %N. It can be
concluded that a time difference of 13,000
years between Eirós (25,000 yBP aprox)
and Liñares (38,000 yBP aprox) remains
has not affected to collagen preservation.
80 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
FFiigguurree 66:: CCaarrbboonn aanndd nniittrrooggeenn ppeerrcceenntt iinn eexxttrraaccttiioonn pprroodduucctt.. LLiinneeaarr rreeggrreessssiioonn ttrreenndd lliinnee ffoorr LLiiññaarreess
((UUrrssuuss ssppeellaaeeuuss aanndd CCeerrvvuuss eellaapphhuuss bboonneess)) eexxppllaaiinnss 9966%% ooff tthhee ssaammppllee vvaarriiaabbiilliittyy,, ssllooppee cclloossee
ttoo 33.
This paper integrates very different
information: isotopic biochemistry, metric
palaeontology, absolute dating, and geo-
morphology with the final result of attai-
ning paleoclimatic reconstructions.
Focused in Ursus spelaeus from Galician
sites, we use the non-suckling group from
Eirós Cave (FERNÁNDEZ, 1998) as iso-
topic reference. As we have reduced the
metabolic causes of variation by using the
same species, same kind of tissue and non
suckling individuals, we could blame
environmental parameters as origin of iso-
topic differences.
In figures 4 and 5, cave bear shows the
lowest δ15N and δ13C values among herbi-
vores (BOCHERENS, 1997; BOCHE-
RENS et al., 1997a). Its low isotopic signal
in bone collagen relates with diet, climate
and physiology,(AMBROSE, 1991). δ13C
from Liñares -as Eirós (FERNÁNDEZ,
1998)- is consistent with an alimentary
chain based in C3plants, under
humid/temperate conditions (BOCHE-
RENS et al., 1991b; BOCHERENS et al.,
Nutritional and hydric stress are
important conditionings for δ13C and δ15N
isotopic signals. In order to avoid the
influence of metabolic parameters, it is
really crucial to keep in mind different
requirements as: choosing the same spe-
cies, tissue and age stage. Nevertheless,
some previous works (see table 2) have
used time intervals too large and thus,
influence of metabolic parameters cannot
be discriminated.
In this work, Liñares data (occupation
around 38-40,000 y BP and 1,115 m
above sea level), and Eirós ones (around
25,000 y BP and 715 m a.s.l.) have been
compared. It must be granted that, once
eliminated the metabolic influence in
δ15N, differences in this signal (between
Liñares and Eirós) correspond exclusively
to environmental factors.
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 81
1. Eirós (suckling) [-22.79 to -21.06] [5.16 to 9.96] * 25
2. Eirós (non suckling) [-22.22 to -20.44] [3.85 to 6.94] 24,090 ± 440 yBP ζ23
3. Liñares [-21.72 to -20.63] [2.11 to 3.61] > 38,000 yBP ζ20
35,000 ± 1,440 yBP) ζ
TTaabbllee 22:: IInntteerrvvaallss ffoorr GGaalliicciiaann ccaavvee bbeeaarr δδ1133CC aanndd δδ1155NN vvaalluueess.. ((11,, 22)) FFEERRNNÁÁNNDDEEZZ,, 11999988.. [[nn]] SSaammppllee ssiizzee..
[[ζζ]] DDaattiinnggss bbyy 1144CC AAMMSS bboonneess.. [[**]] SSaammee ssttrraattiiggrraapphhiicc lleevveell tthhaatt nnoonn ssuucckklliinngg,, ssoo iitt iiss aassssuummeedd tthhee
ssaammee aaggee tthhaatt tthhee E
Eiirróóss nnoonn--ssuucckklliinngg ggrroouupp..
According to previous literature, there
is a good correlation between low δ15N
values and forestry habitats (BOCHE-
RENS et al., 1994). Lower values for δ15N
(as Liñares) are related to cool and wet con-
ditions. As the assumption of a dense
forest, with cold and humid soils, is made
from a present point of view, it would be
naïve to suppose that Liñares individuals
lived in a colder phase than Eirós inhabi-
tants. Initially, Liñares and Eirós sites are
so close that would not seem very real to
establish strong climatic differences bet-
ween these two sites. Then, δ15N differen-
ces between Eirós and Liñares (see figure 5)
point out minor thermic optima in the last
glacial phase (see figure 7). This means
good conditions for N2-fixer-organisms
activity, allowing shrubs and maybe trees
to grow in the higher settlement (Liñares).
82 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
+5 0-5 -10 Isotopic
Glacial data
Temperature (ºC)
Age (thousand years)
Ursus spelaeus (24.090 ± 440 BP)
Inner drumlin
15,465 ± 6,991 BP
(Q4) Queixa
Outer drumlin
21,646 ± 16,963 BP
(Q3) Queixa
Frontal moraine complex
126,184 ± 13,260 BP (Q2) Queixa
Difluent valley
130,732 ± 16,838 BP (AX1) Xurés
Speleothem (28,233 ± 5.027 BP) Eirós
Ursus spelaeus (35,230 ± 1.430 BP) A Ceza
Ursus spelaeus (35,000 ± 1.440 BP) Liñares
Ursus spelaeus (>38,000 BP) Liñares
Cervus elaphus (>38,000 BP) Liñares
Homo sapiens sapiens (210 ± 70 BP) Arcoia
Ursus arctos (7,460 ± 95 BP) Tarelo
(1,795 ± 75 BP) Doniños
(3,970 ±50 & 4,350 ±90 BP) Seselle
(4,135 ± 80 BP) Puerta Real
(12,275 ± 95 BP) Ares
(8,990 ± 400 BP) Lucenza
(13,400±400 BP)
Laguna Grande
(23,300±400 BP) Villaseca
(25,000 BP) La Mata
sedimentary data
Frontal moraine complex:
Chaguazoso (Queixa)
Lagoa de Marinho (Gerês)
Prada-II (Queixa)
Moraine complex from:
Fafião (Gerês)
Fecha (Gerês, Xurés)
Vilamés (Gerês, Xurés)
Castiñeiras y Prada-I (Queixa)
Slope series:
(37,505 ± 1.925 BP) Sorrizo
(38,000 BP) Leira
(>38,000 BP) Rañal
Speleothem (117,252 ± 75,438 BP) Eirós
Speleothem (97,051 ± 15,426 BP) Eirós
Cervus elaphus (17,720 ± 185 BP) Liñares
More or less 38-40,000 y BP, climate
would be in a warm/soft short phase (inside
a general cooling corresponding to the last
glacial phase, see figure 7). At this
moment, around Liñares cave could exist a
kind of C3 vegetation which is now reflec-
ted, as basement of trophic chain, in Ursus
spelaeus signals. As signal δ15N is lower
than Eirós one, we understand that
atmospheric-nitrogen fixation should be
very active due to better conditions for
this process. Soil acidity and soil age, with
influence in soil δ15N are equivalent in
both sites. Non-suckling δ15N data agree
with colder conditions: limitation in N2-
fixers activity when parameters as tempe-
rature and available liquid water decrease.
Liñares site is demonstrated as Ursus
spelaeus refuge around 35,000 yBP
(GRANDAL & LÓPEZ, 1998). Its occu-
pation does not correspond with Eirós one
(approximately 25,000 yBP). The former
felt more influence of glacial conditions
(even when both were out of glacial-ice-
limits) because of its altitude and location
(GRANDAL et al., 1997). It is consistent
to suppose that when weather conditions
were so hard to prevent a normal activity
of cave bears -we guess around 25,000
yBP- they would descend from sites as
Liñares to easier stuffs as Eirós.
As figure shows 7, Liñares occupation
(40,000 yBP aprox.) would be located insi-
de Isotopic Stage 3. That age coincides
with a wet climate, warm enough to allow
the growing of significant taxa in moun-
tains. On the other side, Eirós term would
belong to Isotopic Stage 2, when all refe-
rences show a hardening in conditions at
the highest locations of the Courel Sierra.
The soft phase in Isotopic Stage 3 agree
with some polinic records at lower altitude
(FERNÁNDEZ et al., 1991 and RAMIL,
1992 In PÉREZ & RAMIL, 1996).
Isotopic biochemistry data support the
theory of herbivore diet for Ursus spelaeus
due to low δ15N and δ13C values.
This isotopic study does not consider
other factors than environmental ones due
to sample selection (see Sample and
Techniques). The studied sample corres-
ponds to different sites, Liñares and Eirós,
with a non contemporaneous animal occu-
pation (GRANDAL & VIDAL, 1997;
LÓPEZ & GRANDAL, 1998). We
understand the significant differences in
δ15N as caused by environmental changes.
As N2fixation raises during a warm
event included in a glacial period, it can
be identified a a warm phase around
40,000 yBP (Isotopic Stage 3) included in
the last glacial event for NW Iberian
Peninsula. Then, caves as Liñares (1,115
m.a.s.l.) were occupied by Ursus spelaeus.
Around 25,000 y BP (Isotopic Stage 2)
the climate changed towards colder condi-
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 83
FFiigguurree 77..-- PPaalleeoocclliimmaattiicc rreeccoonnssttrruuccttiioonn ffoorr LLaattee
PPlleeiissttoocceennee iinn NNWW IIbbeerriiaann PPeenniinnssuullaa.. OOnn
tthhee lleefftt,, ggl
loobbaall tthheerrmmiicc rreeffeerreennccee ccuurrvvee
ffrroomm VVoossttookk iiccee ccoorree ((mmooddiiffiieedd ffrroomm JJOOUU--
ZZEELL eett aall..,, 11998877 IInn AANNDDEERRSSEENN &
BBOORRNNSS,, 11999944)).. DDaattaa ffrroomm ddiiffffeerreenntt ssuubb--
jjeeccttss aaggrreeee wwhheenn ddeeffiinniinngg cchhaannggeess iinn ppaallee--
ooeennvviirroonnmmeennttaall cco
((FFEERRNNÁÁNNDDEEZZ,, 11999999;; VVIILLAA,, 11999999))..[[11]]
LLaaggoooonn,, [[22]] RRiiaa bboottttoomm sseerriieess,, [[33]] GGllaacciiaall
84 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
tions and individuals moved to lower sites
as Eirós (780 m.a.s.l.).
Global references as the Vostok ice core
prove that the alternation -cold and warm
phases- pattern included in the last glacial
event and inferred by the paleontological iso-
topic record of Eirós and Liñares is feasible.
This paper is a contribution to the
Research Project XUGA10308A97.
Laboratorio Xeolóxico de Laxe has provided
with a high valuable sample in order to
carry this work out. Juan Ouro was really
patient with our computer doubts.
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 85
(1994). The Ice Age World. An introduc-
tion to Quaternary History and Research
with Emphasis on North America and
Northern Europe during the last 2,5
Million Years. Scandinavian University
Press, Oslo.
ANDERSON, T. (1992). Black Bear.
Seasons in the Wild. Voyageur Press,
Inc. Minnesota.
AMBROSE, S.H. (1991). Effects of Diet,
Climate and Physiology on Nitrogen
Isotope Abundances in Terrestrial
Foodwebs. Journal of Archaeological
Science, 18: 293-317.
(1989). Climate and Habitat
Reconstruction Using Stable Carbon
and Nitrogen Isotope Ratios of
Collagen in Prehistoric Herbivore
Teeth from Kenya. Quaternary Research,
31: 407-422.
J.P. & BELLON G. (1991a). Isotopic
biogeochemistry (δ13C, δ15N) fo fossil
vertebrate collagen: application to the
study of a past food web including
Neandertal man. Journal of Human
Evolution, 20: 481-492.
NE, S. (1991b). Biogéochimie isotopi-
que (δ13C, δ15N, δ18O) et paléoécologie
des ours pléistocènes de la grotte
d’Aldène. Bulletin du Museé
Antropologuique et Prehistorique. Monaco,
36: 29-49.
MARIOTTI, A. (1994). Diet, physio-
logy and ecology of fossil mammals as
inferred from stable carbon and nitro-
gen insotope biogeochemistry: impli-
cations for Pleistocene bears.
Palaeogeography, Palaeoclimatology,
Palaeoecology, 107: 213-225.
TUROSS, N. & ZEDER, M. (1995).
Trophic structure and Climatic
Information from isotopic signatures
in Pleistocene cave fauna of Southern
England. Journal of Archaeological
Science, 22: 327-340.
BOCHERENS, H. (1997). Alimentation
des ours et signatures isotopiques.
L’homme et l’ours/Man and bear
Internation Meeting, 4-6 Nov. GIRPPA.
(1997a). Diagenetic evolution of mam-
mal bones in two French Neolithic
sites. Bulletin de la Socièté Géologuique de
France, 168 (5): 555-564.
(1997b). Paleobiological implications
of the isotopic signatures (δ13C, δ15N) of
fossil mammal collagen in Scladina
Cave (Sclayn, Belgium). Quaternary
Research, 48: 370-380.
(1994). Stable isotopes of nitrogen and
carbon of North American white-tai-
led deer and implications for paleodie-
tary and other food web studies.
86 Vila Taboada, et al. CAD. LAB. XEOL. LAXE 24 (1999)
Plaeogeography, Palaeoclimatology,
Palaeoecology, 107: 227-241.
DE NIRO, M.J. (1985). Post mortem pre-
servation and alteration of in vivo bone
collagen isotope ratios in relation to
palaeodietary reconstruction. Nature,
317: 806-809.
Biogeoquímica isotópica (δ13C, δ15N) del
Ursus spelaeus del yacimiento de Cova Eirós,
Lugo. Cad. Lab. Xeol. Laxe, 23: 237-249.
Aplicación de los nucleidos cosmogénicos a
la datación de procesos geológicos. Tesis de
licenciatura. Universidade da Coruña,
114 pp. No published.
Estudio paleontológico de los restos de Ursus
1794 (Mammalia, Carnivora, Ursidae)
de Cova Eirós (Triacastela, Lugo, NW de
la Península Ibérica). Tesis Doctoral.
Universidade da Coruña, 256 pp.
ROMANÍ, J.R. (1997). A population
study on the Cave Bear (Ursus spelaeus
ROS.-HEIN.) from Cova Eirós
(Triacastela, Galicia, Spain). Geobios,
30 (5): 723-731.
J.R. (1997). Condicionantes en la dis-
tribución de macromamíferos en
Galicia (NW Península Ibérica) duran-
te el Cuaternario superior. Cad. Lab.
Xeol. Laxe, 2222: 43-66.
GONZÁLEZ, F. (1998). A population
study on the Cave Bears (Ursus spelaeus
Rosenmüller-Heinroth) from Galician
caves, NW of Iberian Peninsula. Cad.
Lab. Xeol. Laxe, 23: 215-224.
A. & LONGINELLI, A. (1997). A sta-
ble isotope study of fossil mammal
remains from the Paglicci cave,
Southern Italy. N and C as palaeoenvi-
ronmental indicators. Earth and
Planetary Sciencie Letters, 148: 349-357.
N. (1994). Tracing the diets of fossil
animals using stable isotopes. In: Stable
Istopes en Ecology and Environmental
Science. Lajtha, K. & Michener, R.H.
(Eds.) Methods in Ecology Serie.
Blackwell Scientific Publications
KURTÉN, B. (1976). The Cave Bear Story.
Life and Death of a Vanished Animal.
Columbia University Press. New York.
(1994). Introduction. In: Stable Isotopes in
Ecology and Environmental Science. Lajtha
& Michener Eds. Methods in Ecology
Serie. Blackwell Scientific Publications.
LAJTHA, K. & MARSHALL, J.D. (1994)
Sources of variation in the stable isoto-
pic composition of plants. In: Stable
Istopes in Ecology and Environmental
Science. Lajtha, K. & Michener, R.H.
(Eds.) Methods in Ecology Serie.
Blackwell Scientific Publications.
LÓPEZ GONZÁLEZ, F. (1996). Estudio
geomorfológico y paleontológico del endocarst
de Liñares S (Lugo). Tesis de
Licenciatura. Universidade da Coruña,
90 pp. No published.
J.R. (1997). Análisis tafonómico de la
CAD. LAB. XEOL. LAXE 24 (1999) Paleoecological implications 87
muestra ósea de Liñares sur (Lugo,
Galicia). Cadernos do Laboratorio Xeolóxico
de Laxe, 22: 67-80.
d’ANGLADE, A. (1998). Datos sobre
Cervus elaphus (Cervidae, Artiodactyla,
Mammalia) en cavidades cársticas de
Galicia (NW España). Cadernos do
Laboratorio Xeolóxico de Laxe, 23: 201-213.
MILTON, J.S. (1994). Estadística para
Biología y Ciencias de la Salud. 2ª edición cas-
tellana. Ed. McGraw-Hill-Interamericana
de España. Madrid.
CODE, C.F. (1975). Nitrogen metabo-
lism in bears: urea metabolism in sum-
mer starvation and in winter sleep and
role of urinary bladder in water and
nitrogen conservation. Mayo Clinic
Pro., 50: 141-146.
P. (1996). La evolución bioclimática y
sus consecuencias: el ejemplo de los
paleopaisajes del Cuaternario en
Galicia. Gallaecia 14/15: 31-66.
(1996). δ13C Analysis of Cholesterol
Preserved in Archaeological Bones and
Teeth. Analitical Chemistry, 68: 4402-
Stable carbon and nitrogen isotope
ratios of individual aminoacids give
new insights into bone collagen degra-
dation. Bulletin de la Socièté Géologuique
de France, 169 (1): 109-114.
(1993). Ancient proteins in fossil
bones. Methods in Enzymology, 224:
VIDAL ROMANÍ, J.R. (1996).
Geomorfología de Galicia. In: Historia
de Galicia. Tomo de Xeografía. Hércules
de Ediciones. A Coruña, pp: 7-67.
VILA TABOADA, M. (1998). Nota sobre
el estudio de ADN antiguo en restos
óseos de macromamíferos cuaternarios
de Galicia. Cadernos do Laboratorio
Xeolóxico de Laxe, 23: 263-270.
VILA TABOADA, M. (1999).
Paleontología molecular: Nuevas herra-
mientas para el estudio de restos óseos de
macromamíferos cuaternarios. Tesis de
licenciatura. Universidade da Coruña,
236 pp. No published.
WANG, Y. & CERLING, T.E. (1994). A
model of fossil tooth and bone diage-
nesis: implications for paleodiet
reconstruction from stable isotopes.
Palaeogeography, Palaeoclimatology,
Palaeoecology, 107: 281-289.
... The bear species of the Mammoth Steppe identified as meat-eaters based on their relatively high δ 15 N values were the extinct short-faced bear (Arctodus simus) in eastern Beringia, with a specialized diet on reindeer (Fox-Dobbs et al. 2008, Yeakel et al. 2013, and the brown bear (Ursus arctos) in Europe . In contrast, the cave bear (Ursus spelaeus), exclusive to Europe, systematically had relatively low δ 13 C and δ 15 N values as the result of a vegetarian diet (e.g., Bocherens et al. 1997Bocherens et al. , 2006Bocherens et al. , 2011aBocherens et al. , 2011bBocherens et al. , 2014aNelson et al. 1998;Vila Taboada et al. 1999;Terlato et al. 2019). Over all tested locations in Europe, only a few specimens in Romania with high δ 15 N values appeared to be an exception to this herbivorous diet (Richards et al. 2008, Robu et al. 2013, Krajcarz et al. 2016. ...
The Mammoth Steppe was the dominant terrestrial biome of the Northern Hemisphere during the late Pleistocene. It encompassed a nonanalog community of animals living in a cold and treeless steppe-tundra landscape. The high diversity of species, including megafauna, could be supported by a productive environment. The carbon-13 and nitrogen-15 abundances in bone collagen confirmed that the coexistence of the large herbivores was facilitated by a pronounced dietary niche partitioning, with some species relatively flexible in the exploitation of browse and graze, while others were more specialized. The isotopic abundances of carbon and nitrogen in carnivores confirm a dietary partitioning, probably based on the size of prey, with an increasingly generalist behavior emerging after the Last Glacial Maximum with notable exceptions. Isotopic investigation reveals dynamic processes of ecological displacement and replacement, shedding new light on the potential niche spectrum of extant species that are now present as relic populations. ▪ The Mammoth Steppe is an extinct nonanalog ecosystem with high productivity and biodiversity despite the cold and dry conditions of the Last Glacial Period. ▪ Stable isotopes reveal that niche partitioning among herbivores and carnivores is a dominant trait of the Mammoth Steppe. ▪ Switches in preferred prey and ecological replacement are observed among carnivores over time, with the few highly specialized predators going extinct. ▪ Warmer and more humid conditions preceding the Holocene impacted large herbivores in most regions of the Mammoth Steppe, driving some of the largest ones to extinction. Expected final online publication date for the Annual Review of Earth and Planetary Sciences, Volume 50 is May 2022. Please see for revised estimates.
... Radiocarbon dates from Cova dos Santos (symbols with black border) and other radiocarbon dates from Galicia (data from:Vila-Taboada et al., 1999;Pérez-Rama et al., 2011;López-Costas et al., 2015;García-Vázquez et al., 2015, 2018Fortes et al., 2016;Grandal-d'Anglade & Vidal-Gorosquieta, 2017;Grandal-d'Anglade et al., 2019) with reference to the climate curve ofAndersen et al. (2004). ...
Full-text available
Cova dos Santos is a karstic cavity in Abadín (Lugo), in a hitherto unexplored area that may have been the natural route between the well-known Quaternary faunas of the Cantabrian Mountain Range and those located further south in Galicia, such as in the Serra do Courel. The surface surveys carried out during the topographic layout revealed the presence of deposits of bone remains, usually extremely fragmented, of medium and large vertebrates. Due to the nature of these remains, different molecular techniques (ZooMS, stable isotopes), radiocarbon dating, and morphological and metric analysis were used to characterise the remains present at the site. Combining these methods, it has been possible to identify different taxa such as Ursus speleaeus, Ursus arctos, Panthera pardus, Cervus elaphus, Rhinocerotidae, and to confirm the occupation of this cave since at least 43000 years ago calBP. The presence of domestic species, such as Ovis aries, Equus sp. and Gallus gallus, also shows the use of this cave in more recent times.
... Graf 4. Hodnoty stabilného izotopu δ 13 C z kolagénu kostí medveďov jaskynných zo študovaných lokalít (žltá) a z vybraných jaskýň Európy a Severnej Ameriky (podľa Katzenberg, 1989;Bocherens et al., 1992Bocherens et al., , 1994Bocherens et al., , 1997Bocherens et al., , 1999Bocherens et al., , 2004Bocherens et al., , 2006Matheus, 1995;Fernandez-Mosquera, 1998;Nelsona et al., 1998;Vila-Taboada et al., 1999;Bocherens, 2000;Richards et al., 2000Richards et al., , 2008Fernandez-Mosquera et al., 2001;Baichtal, 2003). ...
Full-text available
This thesis present an image of paleoclimatic and paleoenvironmental conditions of Slovakia and Moravia during time span from 52 000 to 8 000 years BP (OIS 3 – OIS 1; Oxygen isotope stage 3 – Oxygen isotope stage 1) (from middle part of Last Glacial to lower Holocene) on the base of stable isotope analyses. Isotope study of carbon, oxygen and strontium (13C/12C, 18O/16O, 87Sr/86Sr) of the Mammuthus primigenius tusks (Moravia: Předmostí – Přerov II., Brno – Vídeňská street, Pekárna Cave, Kůlna Cave and the Slovak Republic: Slaninova Cave, Trenčianske Bohuslavice – Pod Tureckom, Dzeravá skala cave), Ursus spelaeus and Ursus ex gr. spelaeus teeth (Slovak Republic: Tmavá skala Cave, Medvedia Cave – Západné Tatry, Medvedia Cave – Slovenský raj, Važecká Cave and Cave of Izabela Textorisová), Equus sp. teeth (Moravia: Balcarka Cave, Pekárna Cave, Býčí skála Cave, Kolíbky Cave and Smolín) and Rangifer tarandus teeth (Balcarka) were used for recording of short-term climatic fluctuations and for interpretations of ecosystem evolution, reconstruction of migration, paleodiet, paleovegetation and paleotemperature./ Key words: Isotopes, Mammuthus primigenius, Equus sp., Rangifer tarandus, Ursus spelaeus, Ursus ex gr. spelaeus, Paleotemperature, Paleoenvironment, Slovakia, Moravia, Vistulian, Lower Holocene.
... In contrast, other less studied topics were less studied, such as body mass, encephalization, growth patterns and metabolism, representing only 10% of the papers (e.g. Viranta 1994;Nelson et al. 1998;Vila-Taboada et al. 1999;Fernández-Mosquera et al. 2001;Pérez-Rama et al. 2011;Fuchs et al. 2015;Veitschegger 2017). Strikingly, there is a rising interest for this topic during recent years, most probably due to the advantages of new threedimensional analytical tools. ...
In this issue, we cover an exceptional topic in Vertebrate Paleobiology that has been an enjoyable challenge for scientists and the popular media alike: the life and death of the Pleistocene cave bear (Ursus spelaeus). As an icon of the ice-age, the cave bear inhabited the glacial ecosystems of Eurasia, and it was the inspiration of a popular book written in 1976 by Björn Kurtén, entitled The cave bear story: life and death of a vanished animal. Although ‘The life and death’ was a summary of the knowledge acquired on cave bear biology at that time, four decades later, many aspects of its palaeoecology, extinction and evolution are still a matter of debate. With this volume, we aim to bring together the most recent research on cave bear biology in order to provide an update on the palaeoecology, biogeography, systematics, and phylogeny of this recently extinct ursine bear. We thus organised a symposium on the 1st of August 2017 as part of the three-day Annual Meeting of the European Association of Vertebrate Palaeontologists (EAVP) in Munich, Germany, that was an additional opportunity to announce the volume and to discuss this exciting subject face-to-face among specialists.
... Diet reconstructions in extinct organisms can be based on a multitude of approaches , and the diet of the cave bear has been analysed using stable isotopes ( 13 C/ 12 C; 15 N/ 14 N) preserved in teeth and bones (e.g. Bocherens et al. 1994Bocherens et al. , 1997Fernandez-Mosquera 1998;Nelson et al. 1998;Vila Taboada et al. 1999;Fernandez-Mosquera et al. 2001;Bocherens 2018;Robu et al. 2018), functional morphology of its craniodental morphology (Figueirido et al. 2009;van Heteren et al. 2009van Heteren et al. , 2014van Heteren et al. , 2016 or dental microwear (Pinto-Llona 2006;Peigné et al. 2009a;Münzel et al. 2014;Jones and DeSantis 2016). Accordingly, as different techniques provide information on different aspects of the cave bear diet, it is always important to combine information from different sources to better understand its feeding behaviour. ...
The diet of the cave bear (Ursus spelaeus) is a controversial topic, as different paleobiological approaches (e.g. dental wear, isotopic biochemistry, skull morphometrics) result in different dietary inferences for the cave bear, ranging from carnivory to pure herbivory. Here, we review the main results obtained from these approaches, with special emphasis on those obtained from the morphometric analyses of the cave bear craniodental skeleton. Then, we compute a between-group Principal Components Analysis from a set of 3D-landmarks digitized on 103 mandibles of living bears and extinct cave bears and using a phylomorphospace approach. Moreover, we also reconstructed the evolutionary trajectory of the cave bear mandible from the hypothetical shape of its inferred ancestor. Our results indicate that the mandible of the cave bear possess specific traits indicative of a highly-herbivorous diet or, at least, more herbivorous than their closest living relative, the brown bear (Ursus arctos). Moreover, we also propose new directions for future research to obtain more detailed inferences on the potential food resources consumed by the cave bear being crucial to understand the ‘life and death’ of this vanished animal.
... In fact, the diet of the cave bear represents an interesting case in which different analytical methodsor even the same methods performed on different populationsapparently give disparate conclusions. In fact, traditional studies based on functional morphology (Kurtén 1967;Mattson 1998) as well as more recent analyses based on 3D geometric morphometrics of the skull (Van Heteren et al. 2009, on isotopic biochemistry (δ 13 C/δ 15 N) of bones and teeth (Bocherens and Mariotti 1997;Bocherens et al. 1999;Vila Taboada et al. 1999;Bocherens et al. 2006Bocherens et al. , 2011Bocherens 2018), and on feeding biomechanics (Grandal-d'Anglade et al. 2010) indicate a highly herbivorous diet for the cave bear. However, 2D morphometric analyses (Figueirido et al. 2009), taphonomic evidence (Pinto Llona and Quilès et al. 2006;Pacher and Stuart 2009), dental microwear (Peigné et al. 2009;Peigné and Merceron 2017) as well as biogeochemical analyses performed on specific populations (Richards et al. 2008;Robu et al. 2018) suggest a more omnivorous diet for the cave bear, similar to the one of the living brown bear (Ursus arctos). ...
Full-text available
The morphology of both crowns and tooth-roots reflects dietary specialisation in mammalian carnivores. In this article, we analyse the tooth-root morphology of maxillary teeth from CT scans of living bears (Ursus arctos, Ursus americanus, Ursus maritimus, Ursus thibetanus, Melursus ursinus, Helarctos malayanus, Tremarctos ornatus and Ailuropoda melanoleuca) in order to make inferences about the diet and feeding behaviour of the extinct cave bear (Ursus spelaeus sensu lato). Specifically, we investigate two major mitochondrial clades of extinct cave bears recognized by previous authors: Ursus ingressus and Ursus spelaeus (U. spelaeus spelaeus, U. spelaeus ladinicus, U. spelaeus eremus). Our results indicate a close association between tooth-root surface area and feeding behaviour in all living bear species. Tooth-root surface area values of cave bears suggest that they relied more on vegetative matter than living brown bears (Ursus arctos) but subtle differences between these species/subspecies could also indicate different feeding strategies among the members of cave bear complex.
... Understanding feeding habits of cave bear is essential as it might give insight into those factors contributing to their extinction: whether they were strictly herbivores or more flexible omnivores could have resulted in different scenarios, whereby the relative influence of climate change, human pressure could have played different roles (Pacher & Stuart, 2009;Bocherens et al., 2014a). In this context, herbivorous feeding habits inferred from tooth, skull and jaw morphology (Kurté, 1976;van Heteren et al., 2016) as well as the stable isotopic composition of cave bear collagen from a large majority of European sites, ranging from Spain to Romania, indicate an essentially vegetarian diet (Bocherens et al., 1997;2006;Vila Taboada et al., 1999;Grandal-d'Anglade et al., 2011;Münzel et al., 2011;Horacek et al., 2012;Pacher et al., 2012;Krajcarz et al., 2016;Naito et al., 2016). In contrast, δ 13 C and δ 15 N analyses on cave bears from two Romanian sites (Richards et al., 2008;Robu et al., 2013) suggested that some cave bears included a substantial amount of meat in their diet. ...
We present here the chronometric, isotopic and taphonomic evidence of cave bear from three Palaeolithic sites in north-eastern Italy: Paina, Trene and Buso doppio del Broion (Berici Hills - Vicenza). Two direct radiocarbon dates yielded an age around 24 ka BP, which make these remains the latest known representatives of the species in Europe and confirmed that demise of cave bear falls during the LGM. The carbon and nitrogen isotopic values of bone collagen do not show any marked ecological change since 33 ka BP, suggesting an essential vegetarian diet. Several bear bones preserved traces of human modification such as cut marks, which en-ables a reconstruction of the main steps of butchering process. © 2010 AIQUA - Associazione Italiana per lo Studio del Quaternario e EMMEVI - Servizio Congressi SPA.
... Further isotopic analyses of cave bears from other areas in Western and Central Europe such as France, Spain, Germany, Belgium, Austria, as well as in the northern Caucasus, confirmed this view (e.g. Bocherens et al. 1997Bocherens et al. , 2001Bocherens et al. , 2006Bocherens et al. , 2011bBocherens et al. , 2014aFernandez Mosquera 1998;Vila Taboada et al. 1999;Münzel et al. 2011; Bocherens 2015) ( Figure 1). In parallel, it was also recognised that some physio- logical aspects, such as milk suckling, growth and hibernation, also had an impact on the isotopic values measured on fossil bears and could interfere with the paleodietary interpretations (e.g. ...
More than 300 cave bear bones from all over Europe have carbon and nitrogen isotopic composition that match overwhelmingly a diet based on plants, except for samples from two caves in Romania, for which high nitrogen-15 amounts have been interpreted as reflecting an omnivorous diet. This paper aims at deciphering the various factors influencing the carbon and nitrogen isotopic composition of a potential omnivorous species like cave bear, those linked to trophic levels and variations among plants and those caused by physiological factors. The comparison of European cave bears with coeval Late Pleistocene large mammals with different diets clearly shows that all the cave bear populations, including those from Romania, present isotopic values overlapping with herbivores, not with carnivores. Therefore omnivory is very unlikely for cave bears. Consumption of plants with high δ¹⁵N values, such as graminoids, forbs and possibly fungi, could explain in part the observed isotopic pattern. In addition, the variations in δ¹⁵N values through ontogeny support the hypothesis of a different hibernation pattern for the Romanian cave bears with high δ¹⁵N values. Future investigations using new isotopic approaches, especially nitrogen isotopic composition of collagen amino acids, should contribute to decipher the paleoecology of these Romanian cave bears.
... Zarówno szczegóły budowy czaszki i zębów, jak i wyniki analiz izotopowych są intepretowane jako dowody świadczące za jego roślino- żernością (np. Kurtén 1976, Mattson 1998, Bocherens et al. 1994, Vila et al. 1999, Fernández-Mosquera et al. 2001) lub wszystkożernością (np. Hilderbrand et al. 1996, Pinto Llona & Andrews 2004, Richards et al. 2008, Figueirido et al. 2009, Peigné et al. 2009, Dotsika et al. 2011, Robu et al, 2013). ...
Equifinality constitutes a challenge when interpreting agency in archaeological sites. The fact that a specific type of damage frequently cannot be linked to a single actor, behavior, or ecological context, handicaps correct interpretations of site formation processes. Actualistic studies have been used to address this type of problem by creating models and analogies to infer the processes that occurred in the past and explain the formation processes of fossil faunas found at archaeological sites. Here, we apply this approach using observational data from Arilla et al. (2014) describing the consumption of ungulate carcasses by wild brown bears (Ursus arctos arctos). We focus on a specific type of damage, peeling, which was observed to be one of the most significant modifications of axial skeletal elements of carcasses eaten by bears. This fact was especially relevant because the peeling damage was initially attributed to the feeding activities of primates (humans and chimpanzeesdPan troglodytes) and only anecdotally to other taphonomic agents. The observational data are then applied to Level 4 of Toll Cave (Moi a, Barcelona, Spain), dated to >49,000 14 C BP, which has been interpreted to be a hibernation lair with significant activity by carnivores and sporadic human presence. Rib and vertebral peeling have also been identified at Level 4 bone assemblage, casting doubt on the agent responsible for this damage (effector) in the cave. The aim of our study is to address the equifinality problems that involve peeling as a taphonomical signature in archaeological sites, taking the Pleistocene site of Toll Cave as a case study.
Full-text available
The diagenetic evolution of bones of different mammal species from two French Neolithic sites (around 4,000 BC), Louviers (Eure) and Bercy (Paris), has been studied using different approaches. Global carbon and nitrogen content of bone powders were a good proxy for collagen content; δ13C values of whole bone carbon have been used to detect the presence of humic contaminants; thin sections were investigated to determine the state of preservation of histological structures and to detect staining and microbial alterations. Collagen has been extracted and its yield and C/N ratio have been measured. Both sites are located on the edge of palaeochannels, and bones were recovered from different burial environments. Comparison of the diagenetic alteration in these different depositional environments demonstrates that different mechanisms are involved and lead to very different states of preservation of the histological structures and of the collagen. The results of this study suggest that such sites may be a useful model to understand the early diagenetic alteration stages of much older palaeontological bones deposited in fluvial environments.
Although various stages of decomposition of bone collagen have been reported, the molecular breakdown is still not completely understood. By investigating the stable C and N isotopes of individual amino acids, this study sheds light on the biochemical processes of microbial decomposition. Collagen was extracted from sterilized compact bone of modern martens inoculated with a selection of soil bacteria in order to induce decomposition. Furthermore, this study determined the amino acid composition, overall stable carbon and nitrogen isotope ratios and isotope ratios of the separated individual amino acids of the collagen. For the bulk collagen, the carbon δ-values of the carboxyl groups were measured. This study demonstrates that the δ15N-values of the total collagen were increased, while bulk δ13C-values were decreased. With respect to the individual amino acids, the δ15N-values and especially the δ13C-values were decreased. This general isotopic shift of the individual amino acids is not related to the modification of their amounts given by the amino acid profiles of experimentally modified collagen. As expected, the carbon isotope ratios of the carboxyl group surmount the overall value. The observed modifications of the amino acid spectra seem to be the result of a selective breakdown of larger amino acids by soil microorganisms. A probable cause could be the stereo-specific repolymerization of peptides which can create insoluble macromolecules during diagenesis.
Low β15N values of Würmian cave bear (Ursus spelaeus) bone collagen indicate a strictly vegetarian diet, and negative δ13C values suggest a forested habitat. Tooth collagen δ15N values are about 2%0 higher than bone collagen within one individual, similar to that found in the modern black bear (Ursus americanus). These data suggest an influence of a 15N-enriched milk diet during the synthesis of tooth collagen, which is partly formed before weaning. Thus, tooth collagen δ15N values are not reliable for adult diet reconstruction. Tooth collagen δ13C values are around 1%0 lower than bone collagen, suggesting a 13C-depleted milk diet. A similar pattern of variation is seen in the average δ13C and δ15N values of several individuals from one locality.Enamel carbonate hydroxylapatite δ13C values are low in cave bears (around −14%0) when compared to carnivores (around −12%0) and herbivores (−10%0). This is probably due to lipid use while hibernating during winter. A similar pattern of enamel carbonate hydroxylapatite δ13C values differences is found between Deninger's bear (Ursus deningeri), carnivores and herbivores in 200,000 to 600,000 year old caves, suggesting a similar physiology for both fossil bear species.
Cholesterol preserved in archaeological bones and teeth constitutes an important new source of palaeodietary information. A method is described here for the isotopic (δ13C) determination of cholesterol employing a semiautomated sample preparation procedure and the technique of isotope ratio monitoring/gas chromatography/mass spectrometry (irm/GC/MS). High-temperature gas chromatography (HT-GC) and high-temperature gas chromatography/mass spectrometry (HT-GC/MS) were used to identify the lipids and quantify the cholesterol present in the total lipid extracts. δ13C values are then readily obtained from nanogram amounts (50 ng) of cholesterol resolved and determined directly by high-resolution capillary irm/GC/MS of trimethylsilylated total lipid extracts. The protocol developed allows effective processing of the large numbers of samples essential for palaeodietary determinations. Analytical precision and reproducibility have been assessed through multiple sampling of the same skeleton (femur, 9th century). Comparable δ13C values have been obtained from different skeletal members from the same individual. The utility of the approach is demonstrated through a study of the δ13C values of cholesterol isolated from sections of femoral bones of individuals excavated from cemeteries (dated Saxon to 18th century) at a coastal site in the U.K. The mean δ13C value (−22.2 ± 0.3‰, σ = 0.9) determined for cholesterol in 50 different individuals indicates a strong preference for marine foods by the members of the community extending back over the last 1500 years. A minority of individuals exhibited δ13C values as low as −26‰, indicating preferences for terrestrial rather than marine foodstuffs.
TheC/Nratio and amino acid composition of organic matter extracted from fossil mammal bones from the Paleolithic site at Marillac (Charentes, France) shown that this organic matter comes from collagen.δ13Candδ15Nvalues of known-diet fossil species demonstrate that these values have been preserved through fossilization processes, and that these fossil mammals can be used as ecological references to determine the Neandertal position in the past food web. Initial Neandertalδ13Candδ15N values suggest that he was mostly carnivorous.RésuméLes rapportsC/N et le spectre d'accides amine´s de la matie`re organique extraite des ossements de mammife`res fossiles du site de Marillac (Charentes, France) montrent que cette matie`re organique provient du collage`ne. Les valeurs deδ13Cet deδ15N de mammaife`res fossiles dont le re´gime alimentaire est connu de´montrent que ces valeurs n'ont pase´te´alte´re´es par la fossilisation et donc ces mammifr`es fossiles peuvent servir de standardse´cologiques pour replacer l'Homme de Ne´anderthal dans son re´seau trophique. Les premie`res valeurs deδ13C et deδ15N mesure´es pour cet homme sugge`rent qu'ile´tait essentiellement carnivore.
IntroductionCarbon IsotopesNitrogen IsotopesHydrogen and Oxygen IsotopesConclusions References
A set of 102 tooth and bone samples of Pleistocene age (32,600-13,300 yr BP) belonging to the species Cervus elaphus, Bos primigenius and Equus caballus and coming from the Paglicci cave (Southern Italy) was studied for the carbon (δ13C) and nitrogen (δ15N) isotopic composition of bone and dentine collage and for the carbon (δ13Cc) isotopic composition of tooth enamel carbonate. The amount of collagen extracted from bone and tooth samples (mg/g) was rather variable, representing approximately only 0.5–15% of the collagen present in a fresh bone. However, the loss of an important fraction of the original collagen during diagenesis did not change the in vivo isotopic composition. In general, when the δ13C of both collagen and carbonate and the δ15N of collagen obtained from each level for the three species are compared, wild ox shows the most increased values, deer the most decreased values and horse shows intermediate results. These differences are probably related to distinct diets or to differences in their physiological behaviour. However, the isotopic results suggest that the three species considered lived in an open environment with a diet based on C3 plants. The stratigraphic sequence of light and heavy nitrogen isotope values between 19,000 and 15,000 may be related to shifts from arid to humid conditions, while the overall trend shown by δ13C toward lighter values may be related to a progressive development of a forest habitat.
Stable carbon and nitrogen isotope ratios have been determined for tooth collagen of 27 prehistoric herbivores from a rock shelter in the central Rift Valley of Kenya. Collagen samples whose isotope ratios were not altered by diagenesis were identified using several analytical methods. During the later Holocene, when the climate was as dry or drier than at present, the isotopic compositions of individual animals are similar to those of modern individuals of the same species. During the earlier Holocene, when the climate was wetter than at present, the δ15N and δ13C values are lower than those for their modern counterparts. When diagenetic factors can be discounted and adequate modern comparative data are available, stable isotope analysis of herbivore teeth and bones can be used to evaluate prehistoric climate and habitat conditions.
Diagenesis of structural carbonate in biogenic apatite in the postmortem environment is modeled as a process of water-mineral interaction. Both closed- and open-system model calculations suggest that δ13C of structural carbonate in biogenic apatite is much more resistant to diagenetic modification than δ18O. Apatite structural carbonate retains an original δ13C signal in closed-system diagenesis. For open systems, δ13C of biogenic apatite with very low porosity, such as tooth enamel, can survive most diagenesis and retain a primary isotopic signature. On the hand, δ18O of structural carbonate in biogenic apatite may not be a reliable indicator of the original isotopic ratios, except in a diagenetic system with low temperature and very low water/biomineral ratio.Application of the model to teeth, and carbonate cement in sediments from the Badlands, South Dakota, illustrates that δ13C values of enamel samples preserve the original signal whereas δ13C values of dentine represent varying extents of diagenesis. δ18O values of fossil teeth may record an early or late part of their water-biomineral interaction history during diagenesis.