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Quaternary International 169–170 (2007) 154–165
Paleoclimatic implications of oxygen isotopic variation in late
Pleistocene and Holocene tusks of Mammuthus primigenius
from northern Eurasia
David L. Foxa,, Daniel C. Fisherb, Sergey Vartanyanc, Alexei N. Tikhonovd,
Dick Mole, Bernard Buiguesf
a
Department of Geology and Geophysics, University of Minnesota, 310 Pillsbury Dr SE, Minneapolis, MN 55455, USA
Museum of Paleontology and Department of Geological Sciences, University of Michigan, Ann Arbor, MI 48109, USA
c
Wrangel Island State Reserve, Pevek, 686870, Chukotka, Russian Federation
d
Zoological Institute, Russian Academy of Sciences, Saint Petersburg 199034, Russian Federation
e
CERPOLEX/Mammuthus, Hoofddorp, The Netherlands
f
CERPOLEX/Mammuthus, Saint Mandè, France
b
Available online 13 November 2006
Abstract
To understand the role of climate change in the extinction of Mammuthus primigenius in Eurasia, we examine spatial and temporal
variations in growth increment and oxygen isotope (d18O) profiles of radiocarbon dated mammoth tusks. We serially sampled tusk dentin
in late Pleistocene tusks from the Taimyr Peninsula and Chukotka and Holocene tusks from Wrangel Island for a total of 241 oxygen
isotope analyses from 11 tusks. Most sample series spanned 2–3 years of tusk growth. Differences in mean d18O values among the Taimyr
tusks correlate with d18O values in corresponding intervals in the Greenland ice sheet and with regional paleoclimate reconstructions.
The longitudinal gradient in d18O values of late Pleistocene tusks (0.064%/degree) is similar to the modern meteoric water gradient
(0.064 to 0.048%/degree). The temporal gradient in mean tusk d18O in Taimyr from an interstadial during MIS 3 to a stadial during
MIS 2 (4.0%) is similar to the gradient in easternmost Siberia from an interstadial during MIS 3 to the middle Holocene (4.8%).
Seasonality in Chukotka during the late Pleistocene does not appear to be different from that on Wrangel Island during the Holocene.
Our results suggest that climate change as recorded by d18O values of mammoth tusks may not have been the direct cause of the
extinction of Eurasian mammoths.
r 2006 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction
The causes of the late Pleistocene extinction of diverse
large-bodied mammals, including several species of proboscideans, on the northern continents remain a topic of
debate (Martin and Klein, 1984; MacPhee, 1999; Barnosky
et al., 2005). For many years, the primary end-member
hypotheses explaining late Pleistocene extinctions, originally but no longer exclusively based on the North American
Corresponding author. Tel.: +1 612 624 6361; fax: +1 612 625 3819.
E-mail addresses: dlfox@umn.edu (D.L. Fox), dcfisher@umich.edu
(D.C. Fisher), sv@SV1226.spb.edu (S. Vartanyan), atikh@mail.ru
(A.N. Tikhonov), dickmol@tiscali.nl (D. Mol),
b.buigues@polarcircle.com (B. Buigues).
record, have focused on either climatic and environmental
changes associated with the last glacial–interglacial transition (e.g., Graham and Lundelius, 1984; Guthrie, 1984;
Haynes, 1991; Lister and Sher, 1995) or overhunting by
humans (e.g., Martin, 1967; Whittington and Dyke, 1984;
Alroy, 2001; Fisher, 2001a). More recently, hyperdisease
has been suggested as a cause (MacPhee and Marx, 1997),
and a variety of mixed models combine elements of both
climatic/environmental and overkill models (Owen-Smith,
1987; Haynes, 1991).
In the case of Mammuthus primigenius in Eurasia, Stuart
(1991, 1999, 2005) has suggested a mixed model in which
cooler conditions during the Allerød phase of the Late
Glacial Interstadial (ca. 11.8–10.7 ka, all dates in radiocarbon years before present unless otherwise indicated) and
1040-6182/$ - see front matter r 2006 Elsevier Ltd and INQUA. All rights reserved.
doi:10.1016/j.quaint.2006.09.001
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D.L. Fox et al. / Quaternary International 169–170 (2007) 154–165
the expansion of boreal woodlands led to the restriction of
M. primigenius to refugia in northern Eurasia (Taimyr and
Gydan Peninsulas, the Severnaya Zemlya Archipelago, and
Wrangel Island). Following a brief range expansion into
northeastern Europe during the cold Younger Dryas (ca.
10.7–10.0 ka), radiocarbon dates suggest that the final
extinction of mainland populations in Taimyr happened
during the earliest Holocene and that of the remnant
population on Wrangel Island not until the late Holocene
(ca. 3.7 ka; Vartanyan et al., 1993, 1995; Long et al., 1994).
In this model, the final extinctions were potentially caused
by predation by technologically sophisticated modern
human hunters that prevented migrations by stressed and
reduced populations to physiologically and ecologically
suitable refugia from latest Pleistocene and Holocene
environmental changes.
In this paper, we use combined growth increment
profiles and the stable oxygen isotope composition (d18O)
of serial samples of M. primigenius tusks from the Taimyr
Peninsula, Chukotka (easternmost Siberia), and Wrangel
Island, in conjunction with previously published isotopic
results for mammoths from European Russia and central
Siberia (Genoni et al., 1998), to explore aspects of climate
change in northern and eastern Eurasia from the MIS 3
(Middle Weichselian) to the Middle Holocene (6.6–4.2 ka).
Our approach allows us to examine temporal and spatial
changes in both mean annual conditions and seasonal
variation. This work is part of a larger project using growth
increment and stable isotope profiles to understand both
the paleobiology and the extinction of mammoths in
Eurasia. Although the set of dated and analyzed tusks is
relatively small at present (n ¼ 11), the results suggest
several climatic patterns that bear on the role of climate in
the extinction of mammoths in northern Siberia. As the
number of tusks analyzed increases, we will be able to test
the climatic interpretations presented here with additional
oxygen isotope data from both lattice-bound carbonate
and phosphate in tusk apatite and complement the growth
increment and oxygen isotope results with carbon isotope
compositions from apatite carbonate and collagen, nitrogen isotope compositions of collagen, and strontium
isotope compositions of apatite that will provide detailed
paleobiological information. An expanded data set will
also facilitate comparisons with other paleoclimatic and
paleoenvironmental data from the region, such as the d18O
value of permafrost and pollen records.
2. Mammoth tusks and tusk growth
Tusks are highly modified incisor teeth that form
through a life-long history of growth, in response to
complex interactions involving climate, food resources,
behavior, and reproductive history (Fisher, 2001a; see also
Rountrey et al., this volume). They are composed
principally of dentin and cementum. Cementum is initially
present over most of the tusk, but only as a thin, outer zone
which is later reduced or removed by abrasion. The main
155
tusk tissue is dentin, which is a composite material
composed of hydroxyapatite, collagen, small proportions
of other proteins, and water. Geometrically, tusks are
stacks of cone-shaped layers added sequentially from tip to
base. Tusk dentin is composed of a hierarchy of structural
increments that parallel the conical pulp cavity and form
on annual (first-order), weekly (second-order), and daily
(third-order) timescales (Fisher, 2001a). The annual nature
of first-order increments has been corroborated by d18O
profiles in previous studies of serial samples of tusk dentin
(Koch et al., 1998; Fisher et al., 2003; Fisher and Fox,
2003). First-order increments are reproducible within and
between individuals and are identifiable by a variety
criteria in addition to d18O profiles in individuals from
highly seasonal climates: dentin color, topography of the
dentin-cementum junction, and frequently the pattern of
second-order thickness profiles, which can reflect seasonal
variation in tusk growth rate. In high-latitude mammoths,
the number of second-order increments per year varies
from the typical temperate-latitude frequency of 52 per
year to lower numbers that vary inversely with latitude.
The explanation for this pattern is beyond the scope of this
paper but probably relates to the interaction of different
physiological rhythms associated with tusk growth and
mineralization.
Increases in second-order increment thickness have been
related to the nutritional and health status of the
individual, and profiles of second-order increment thickness, in conjunction with criteria for recognizing first-order
increments, can be used to identify winter–spring boundaries. We use the pattern of second-order increment
thickness profiles from each tusk analyzed to identify the
winter–spring boundary as the end of the thinnest secondorder increment in a series of thin increments associated
with a first-order increment boundary. Second-order
increments provide a well constrained temporal framework
for serial sampling of tusks for oxygen isotope composition
of tusk apatite; the second-order thickness profiles and the
winter–spring boundaries identified from them allow us to
interpret subannual variations in the d18O profiles.
3. Oxygen isotope composition of Siberian mammoth tusk
dentin
Both the lattice-bound or structural carbonate and the
phosphate in mammalian tooth apatite form in oxygen
isotope equilibrium with body water (Bryant et al., 1996;
Iacumin et al., 1996). For this paper, we analyzed the
oxygen isotope composition of structural carbonate in tusk
dentin. The oxygen isotope composition of body water
(d18Obw) in terrestrial mammals is controlled by the
magnitude and composition of oxygen fluxes to and from
body water (Luz et al., 1984; Bryant and Froelich, 1995;
Kohn, 1996). Because the mineralized tissues in large
mammals form at a constant body temperature (Cossins
and Bowler, 1987), the only source of variation in the
oxygen isotope composition of mammalian apatite
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(d18Oap) is the composition of body water (d18Obw). In
mammals that ingest large volumes of water as drinking
water or liquid water in plant stems, d18Obw is sensitive to
the oxygen isotope composition of meteoric water (d18Omw;
Ayliffe et al., 1992; Kohn, 1996). Drinking water is derived
from surface water reservoirs, and its d18O is largely
controlled by d18Omw, with modification through evaporative enrichment in 18O and local hydrologic processes.
Liquid water in the stems of food plants is not fractionated
relative to ground water and also reflects d18Omw (Yakir,
1992), but leaf water in arid environments can be
evaporatively enriched in 18O relative to local meteoric
water and the degree of enrichment increases with aridity
(Sternberg et al., 1989). The effect of enriched leaf water on
mammoth d18Oap values is difficult to evaluate, but d18Oap
values of extant elephants Loxodonta africana and Elephas
maximus have a strong, positive correlation with local
d18Omw, and a least squares regression with local d18Omw as
the independent variable and elephant d18Oap values as the
dependent variable has a slope of 0.94 (Ayliffe et al., 1992).
Additionally, a previous study of phosphate oxygen
isotope variation in bulk samples of late Pleistocene
Eurasian mammoth tusks, teeth, and bones suggests that
mammoth d18Oap values are a reasonable proxy for ancient
d18Omw values based on comparisons with d18O values of
ice wedges and ground ice (Genoni et al., 1998).
Using d18Oap values of serial samples of mammoth tusks
as proxies for d18Omw we can explore both temporal and
spatial variation in d18Omw during the late Pleistocene
across Siberia and temporal variation from the late
Pleistocene to the middle Holocene in easternmost Siberia
(Chukotka and Wrangel Island). A recent study of the
isotopic composition of meteoric water in Siberia (Siberia
Network for Isotopes in Precipitation or SNIP; Kurita et
al., 2004) includes sampling stations to the west and east of
the Taimyr Peninsula (Salekhard and Olenek, respectively)
and a coastal station in Chukotka (Ayon), thus providing
modern precipitation data to assist our interpretations of
mammoth data from central (Taimyr Peninsula) and
eastern (Chukotka, Wrangel Island) Siberia. SNIP also
includes stations in European Russia, which is one of the
regions for which mammoth d18O values have been
published (Genoni et al., 1998).
The three primary controls on the isotopic composition
of meteoric water across Siberia today are precipitation
history of air masses as they move across northern Eurasia
from west to east, water vapor source, and temperature.
We can use d18Oap variations in our sample of mammoths
to examine temporal and spatial variations in these factors
in Siberia during the late Pleistocene and Holocene. At the
continental scale, the primary circulation pattern is west to
east transport of vapor across northern Eurasia from vapor
sources in the Atlantic Ocean and the Norwegian and
Baltic Seas (Kållberg et al., 2005). As an individual air
mass moves across Eurasia, loss of moisture through
continuous or sequential precipitation events leaves the
remaining vapor progressively more depleted in the heavy
isotopes of oxygen (and hydrogen) so that later precipitation events have systematically lower d18O values than
earlier precipitation events (this is known as the continental
effect; Rozanski et al., 1993). As a result of the continental
effect, the primary spatial pattern of variation in modern
d18Omw values is a decrease in mean annual and mean
winter d18Omw values from west to east across Siberia
(Kurita et al., 2004). For interior SNIP stations, the spatial
pattern of mean annual and mean winter d18Omw values
can be accurately predicted by a Rayleigh distillation
model in which d18Omw at a given point along the
trajectory of an air mass is a function of the d18O of
the initial vapor, the fraction of initial vapor remaining,
and the fractionation between vapor and liquid (Kurita
et al., 2004).
In easternmost Siberia (Chukotka and Kamchatka),
mean annual and mean winter d18Omw do not correspond
to the predictions of the Rayleigh model and have less
negative d18O values than expected due to contributions of
moisture from sources other than the Atlantic Ocean and
the Norwegian and Baltic Seas. In easternmost Siberia,
seasonal maps of wind vectors and moisture flux indicate
that winter moisture is not derived from western sources
but instead is derived from the North Pacific, with minor
contributions from the nearby Arctic Ocean (Kållberg
et al., 2005). These air masses have different initial vapor
d18O values than western sources and experience little rainout before delivering moisture to Chukotka, and as a result
have higher d18O values than predicted from the Rayleigh
model assuming only eastward transport of moisture. We
will use both our mammoth d18Oap values reported here
and values from the literature for localities across Russia
and Siberia to examine whether patterns that characterized
the late Pleistocene, particularly the Middle Weichselian
interstadial (Sher et al., 2005), are consistent with this
modern continental effect on meteoric water.
For non-coastal stations, mean annual hydrogen isotope
composition of meteoric water (dDmw), which has a strong,
positive correlation with d18Omw values for the same
samples (r ¼ 0.99), has a strong, positive correlation with
mean annual temperature (r ¼ 0.94; Kurita et al., 2004)
that is similar to the pattern observed globally at mid- to
high-latitude sites (Rozanski et al., 1993). On a seasonal
basis, dDmw (hence d18Omw) for winter precipitation also
has a strong, positive correlation with temperature at
interior stations in Siberia (r ¼ 0.93; Kurita et al., 2004),
but this relationship is much weaker during summer
(r ¼ 0.55) because of a low longitudinal gradient in
summer temperatures across Siberia and the contribution
of moisture from the landscape to air masses (see below).
Given that analysis of second-order growth increments
allows us to identify both annual increments of tusk growth
and the included winter growth portions of each year,
changes in mean tusk d18O values in a given region through
time provide a proxy for changes in mean annual
temperature, assuming that regional atmospheric circulation patterns were basically the same in the past as today.
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Similarly, winter growth d18Oap values provide a proxy for
winter minimum temperature in a given region.
Although the isotopic composition of summer precipitation in Siberia does not correlate as strongly with
temperature as does that of winter precipitation, all
stations do exhibit seasonal variation in isotopic composition in which winter precipitation is depleted in the heavy
isotope of H or O (hence has lower d values) relative to
summer precipitation. Seasonality in the isotopic composition of meteoric water increases from west to east as far as
Yakutsk (Kurita et al., 2004) but is lower further east,
presumably due to the interaction between seasonal
variations in temperature and moisture sources. However,
across more or less all of Siberia, summer precipitation has
lower d18O values than predicted by the Rayleigh
distillation model (Kurita et al., 2004). During warm
summer months, evaporation from soils and evapotranspiration from plants contributes vapor from prior
precipitation to air masses as they move from west to east
across Siberia. The proportion of recycled moisture during
summer is generally greater than 40% and can be greater
than 80% in eastern Siberia (Kurita et al., 2004). Early in
summer, both surface water reservoirs and soil water
include relatively more water derived from melt of snow
from the prior winter, which would be isotopically light.
Recycling of this water into summer air masses today
contributes to low summer d18O values in meteoric water in
eastern Siberia, and the effect is enhanced because
evaporation enriches the vapor in 16O. We will use the
seasonal pattern of d18Oap in tusks to examine changes in
the magnitude and pattern of seasonal variation in d18Omw
in the late Pleistocene of the Taimyr Peninsula and
Chukotka and the middle Holocene of Wrangel Island.
Previous studies of d18Oap profiles in serial samples of
North American mammoths have demonstrated seasonal
variations up to almost 5% that correlate with patterns of
seasonal growth in associated growth increment profiles
(Koch et al., 1998; Fisher et al., 2003). To interpret the
Siberian profiles, we will have to consider both regional
variation in seasonal moisture sources and the possible
role of long-term changes in the amount of recycled
moisture during the summer, including the proportion of
moisture derived from snow melt.
4. Materials and methods
4.1. Tusks
We have dated and analyzed the isotopic composition of
serial samples of three tusks from the Taimyr Peninsula,
two tusks from Chukotka and five tusks from Wrangel
Island; we also include a single value for an additional
dated tusk from the Taimyr Peninsula. We have samples of
additional dated tusks from Taimyr and Chukotka that
have not been analyzed for isotopic composition yet. The
Jarkov mammoth from the Taimyr Peninsula was previously dated by accelerator mass spectrometry (AMS) at
the R.J. van de Graaff Laboratory at Utrecht University,
The Netherlands (Mol et al., 2001). The other tusks from
Taimyr and those from Chukotka were dated by AMS at
the Center for Accelerator Mass Spectrometry at Lawrence
Livermore National Laboratory. The Wrangel Island tusks
were dated conventionally at St. Petersburg State University, Russia (Vartanyan et al., 1995). Radiocarbon dates
for the tusks are reported in Table 1 along with summaries
of the d18O profiles from each tusk.
4.2. Tusk sampling
Tusk analyses reported here derive from well preserved
specimens recovered from permafrost. In some cases the
cementum layer on the outside of a tusk shows evidence of
slight weathering (fine, longitudinal fracturing and lightening of surface coloration) associated with recent exhumation and/or transient exposure at some time in the
past, but in all cases the dentin is solid, dense, creamcolored, and pristine in condition. Specimens from the
Taimyr were collected by CERPOLEX/Mammuthus expeditions and were returned to a base of operations in the
city of Khatanga, northern Taimyr, where they are stored
Table 1
Radiocarbon ages and summaries of serial samples from each tusk
Specimen
Jarkov
2000/210
2000/271
2000/288
ZCHM-16
ZCHM-18
32M
9M
33M
34M
29M
Location
Taimyr
Taimyr
Taimyr
Taimyr
Chukotka
Chukotka
Wrangel I.
Wrangel I.
Wrangel I.
Wrangel I.
Wrangel I.
Age (ka)
20.370.15
33.570.4
42.971.4
42.971.4
44.671.6
49.072.0
4.127110
4.40740
6.19770
6.22750
6.56760
Lab no.
UtC 8137-39
CAMS 105532
CAMS 105537
CAMS 105539
CAMS 110335
CAMS 110327
LU-4448
LU-2756
LU-4468
LU-4471
LU-4449
n
22
27
1
25
39
43
20
20
3
15
26
d18Oap VSMOW
mean71 s.d.
Max
Min
15.371.29
19.370.74
17.6
18.470.74
19.170.91
17.671.35
21.271.04
21.170.92
20.470.29
21.470.51
19.470.88
17.4
20.9
12.6
18.1
20.9
21.1
22.6
23.3
22.6
20.7
22.5
21.7
16.0
17.7
14.8
19.4
19.5
20.2
20.9
18.2
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at ca. 11 1C in an ‘‘ice cave’’ dug into the permafrost.
Specimens from Chukotka and Wrangel Island were
mostly not collected in their entirety, because of logistic
restrictions, but samples were cut from the proximal ends
of tusks and returned to a laboratory setting.
Sampling of the Taimyr tusks was conducted in
Khatanga using a heavy-duty drill and specially designed
coring bits to cut 2-cm diameter cores, perpendicular to the
long axis of each tusk, at a series of positions along the
length of the tusk. Spacing of cores was designed to sample
the entire tusk, providing a comprehensive record of life
history, but at this time, we are reporting data for only a
single core per specimen. An entire core, passing through
the center of a tusk and out the other side, contains a
duplicate record (outer surface to central axis, in each
direction) of ca. 6–10 years of an animal’s life. Finished
cores were enclosed in plastic bags to retard moisture loss
but were allowed to dry slowly over the course of about
one year. A narrow facet was then polished along a medial
or lateral flank of the core to display the orientation of
incremental features. Dentin laminae conform to former
positions of the conical pulp cavity of the tusk and are
organized as a series of nested cones along the tusk’s
structural axis. The apical angle of these cones varies
during the life of the animal and tends to differ between
males and females (larger in females). On the polished facet
a cutting plane is marked to be perpendicular to most, if
not all, laminae in the half of the core from the outer curve
of the tusk. This cutting plane, transverse in anatomical
orientation, is typically at an angle of 7–151 from the long
axis of the core. The core is then sliced (with an Isomet lowspeed, diamond wafering saw) to remove two slabs, each
5 mm thick, from the center of the cylindrical core, leaving
two wedge-shaped ‘‘heels’’, or remainders, on either side.
The heels are used to produce thin sections to document
dentin increments, and the slabs are polished on both sides
before they have any opportunity to deform because of
humidity changes. Polishing proceeds through a series of
carbide-grit, adhesive-backed papers, ending with a slurry
of 5-mm laevigated alumina in kerosene. No water is used
during cutting or polishing, as exposure of dry dentin to
water induces significant volume change, distortion, and
sometimes fracturing.
Samples from Chukotka and Wrangel Island were either
round segments or wedge-shaped sectors cut from the
proximal end of tusks. These were also oriented and sliced
with the Isomet into 5-mm thick slabs perpendicular to
dentin laminae. These again were polished on both sides,
while additional samples were trimmed for thin section
production. In the case of cores and these more irregularly
shaped samples, slabs were doubly polished because we are
looking for the best display of fine, second-order (weekly)
increments to guide the milling of serial isotope samples.
The ease with which incremental features can be traced can
vary unpredictably from one surface to another, so it is
useful to be prepared to sample from either side of the
polished slabs.
4.3. Growth increment analysis
Thin sections made from the ‘‘heels’’ remaining after
slicing tusk cores for production of 5-mm slabs are given a
final high-speed polish with 5-mm laevigated alumina in
kerosene (Fisher, 2001a) and stored in plastic bags in an
air-conditioned environment to minimize moisture uptake.
Prior to microscopic analysis, thin sections are inspected
and boundaries of first-order (annual) features are marked,
based on discontinuities in dentin color, translucency, and
locations of prominent (high-contrast) second-order features. Analysis of dentin increments is performed on a
petrographic microscope, using Optimas 5.2 image analysis
software. A transect overlay is constructed perpendicular
to incremental features, and the dark portion of each
second-order couplet is marked onscreen. Numbers and
positions of second-order increments are exported to a
spreadsheet, compiled (from the multiple transects required
to analyze a given sequence), and graphed to yield profiles
of second-order increment thickness.
Some years from these tusks resemble patterns observed
in temperate-latitude mammoths, with 5273 second-order
increments per first-order increment and 771 thirdorder increments per second-order increment, where
third-order increments can be adequately discerned. In
these cases, we can interpret second-order features as
periodic, and their thickness as a direct measure of shortterm rate of dentin apposition. However, as discussed in
Fisher and Fox (2003), other years in high-latitude
mammoths, including especially the last years of life, often
show fewer than 52 increments and, at least locally within
the year, 1171 third-order increments per second-order
increment. In these cases, we suspect second-order increments do not represent a single period of formation, and to
interpret their thicknesses as a direct measure of tusk
growth rate, we would have to distinguish carefully parts of
the year characterized by different periodicities and impose
an appropriate transformation on measured increment
thicknessses. We are currently developing improved means
of visualizing third-order increments to support such
analyses, but for now, we must work simply with ‘‘raw’’
second-order increment data. This complex system has
been provisionally interpreted as reflecting interaction
between mammoths’ circadian rhythms, responsible ultimately for third-order increments, and other periodicities
associated with dentin mineralization (Fisher, 2001b). The
different modes of organization observed (i.e., ca. 52/yr vs.
o52/yr) may in turn represent times when mammoths were
living below, and north of, the Arctic Circle, where certain
times of the year may be characterized by circadian
rhythms that become free-running, rather than entrained
to 24-h light–dark cues (Fisher, 2001b).
The complication introduced by tracing profiles of
increment thickness when the increments do not reflect a
single periodicity compromises our ability to interpret
increment profiles in terms of tusk growth rate, especially
since we provisionally identify winter as a time when the
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increment period may have been longer, making the
apparent growth rate (i.e., without accounting for the
change in period) greater than it actually was. ‘‘Spring,’’ on
the other hand, would have featured the return of 24-h
light–dark cues, entrained circadian rhythms, shorter
(weekly) second-order periodicity, and thus thinner second-order increments. In terms of growth conditions, this
might still effectively represent ‘‘late winter.’’ At high
latitudes, where the start of the short growing season would
be delayed relative to this transition, we may thus expect a
functional ‘‘winter–spring’’ boundary to be associated with
a transition from thin to thicker second-order increments.
For now, we follow this convention.
4.4. Serial sampling for stable isotope analysis
Temporally discrete samples were extracted in series
from each polished 5 mm thick sample slab under microscopic observation by following incremental features with a
carbide steel dental bit with a cutting head that is 0.6 mm in
diameter and 3.0 mm long mounted in a fixed dental drill.
Milling of sample series began either at the pulp cavity
surface and progressed outward toward the dentincementum junction or (for more distal slabs that did not
have a pulp cavity surface) at a prominent growth line or
set of lines between the axial trace and the dentincementum junction and then in both adaxial and abaxial
directions. For individual samples, the stage was raised to
plunge the bit shallowly into the transverse face of the slab
at one end of the sample path, and the slab was then
translated horizontally on the microscope stage to begin
milling the sample using second order growth increments as
guides to minimize temporal mixing between successive
samples. Raising the stage for successive passes along the
initial shallow sample path increased the depth of the
groove until 40–60 mg of dentin powder had been collected.
Successive samples were begun on opposite edges of the
slab and each sample extended only slightly more than half
way across the slab circumferentially to overlap with the
end of the previous sample along the radial midline of the
slab. With this sampling scheme, each sample position
included both a powder sample from the milled groove and
a block sample from the wall left between successive
samples on either side of the sample block. One aliquot of
each powder sample was processed for the oxygen isotope
analyses of structural carbonate presented here; the
remainder of each powder sample was retained for future
analysis of phosphate oxygen and possibly other analyses
(e.g., strontium isotopic and/or elemental composition).
The block samples were processed for carbon and nitrogen
isotope analyses of purified collagen; these results will be
presented in a separate paper that includes the carbon
isotope data from structural carbonate.
The radial thickness of individual samples was measured
on high magnification (440 ) digital photographs using
NIH Image image analysis software. As samples follow
incremental lines and the tusks are not perfectly circular,
159
the thickness of each sample varies slightly along the
sample path. Sample thicknesses were measured in a radial
transect along the overlap zone for successive samples in
the middle of each sample block where the adaxial margin
of one sample forms the abaxial margin of the next sample
farther from the dentin-cementum junction. The thicknesses of successive samples were added to obtain
cumulative distances from the pulp cavity (expressed in
negative units); isotope results from each sample are
plotted at the middle of its measured thickness. When
plotted in the spatial domain against cumulative distance
from the pulp cavity, the oxygen isotope profile from a
sample slab can be directly compared to the growth
increment thickness profile derived from the thin section of
the same block.
4.5. Stable oxygen isotope analyses
Given the pristine preservation of the dentin in all of
these tusks, we followed the basic protocol of Stephan
(2000) to purify powder samples of collagen-rich apatite for
stable isotope analysis of the structural carbonate. A 25 mg
aliquot of each powder sample was soaked in 2 ml of 2–3%
NaOCl for 24 h to dissolve collagen and any sedimentary
organic matter, then rinsed five times in an excess of
distilled water. The samples were then soaked for 24 h in
2 ml of 0.125 N NaOH to dissolve any humic or fulvic
acids, rinsed an additional five times in an excess of
distilled water, and then freeze-dried for at least 12 h.
Samples were not treated with acetic acid as in the protocol
of Koch et al. (1997) because the tusks are geologically
young and are so well-preserved as to be fresh ivory; thus
we are not concerned with contamination by sedimentary
carbonate. Futhermore, results presented here suggest that
contamination with sedimentary carbonate has not occurred. The carbon and oxygen isotope compositions of the
purified carbonate samples were measured using a Finnigan ‘‘Kiel’’ automatic extraction line coupled to the ion
source of a Finnigan MAT 252 isotope ratio mass
spectrometer in the Stable Isotope Laboratory in the
Department of Geology and Geophysics at the University
of Minnesota. Sample values are normalized to the
compositions of National Bureau of Standards carbonate
standards NBS-18 and NBS-19 and two laboratory
standards, and analytical precision is better than 0.1%.
5. Results
Mean, standard deviation, maximum, and minimum
d18Oap values for the sample series from each tusk are
presented in Table 1 and second-order increment and
d18Oap profiles are presented in Figs. 1–3 for representative
results from the Taimyr Peninsula and Wrangel Island and
for both tusks from Chukotka. We briefly summarize the
results for each region below. The full data set is available
from the corresponding author upon request.
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Fig. 1. Growth increment and d18O profiles for tusk 2000/210 from
CERPOLEX/Mammuthus collections from the Taimyr peninsula (south of
Cape Sablera, Lake Taimyr). Vertical lines with arrows indicate positions
of winter–spring boundaries with the number of second-order increments
indicated. In each plot, earlier portions of life are to the left (i.e., time runs
from left to right).
5.1. Taimyr Peninsula
The Taimyr sample includes tusks from three climatically distinct intervals. Based on the calibration curve of
Fairbanks et al. (2005), the two oldest tusks from the
Taimyr Peninsula, 288 and 271 (for which we only have a
single value currently), are from just after the peak of
interstadial 13 during MIS 3 in the Greenland ice cores, but
before the peak of stadial 13 and Heinrich event 5 in the
North Atlantic (Bond et al., 1993; Dansgaard et al., 1993).
Thus, these tusks correspond to a moderate global climate
state. During this interval, northern Siberia to the east of
the Taimyr Peninsula was characterized by warm steppetundra floras, summers that were dry and warmer than
present, and winters that were colder than present (Middle
Weichselian I; Sher et al., 2005). The single value for 271
(17.6%) is lower than the mean for 288 (18.470.74, 1 s.d.)
but falls well within the range of the more complete series
from 288 (20.9–16.0%). The calibrated age for the next
younger tusk, 210, corresponds to Greenland interstadial 8,
just after Heinrich event 4 (Bond et al., 1993; Dansgaard et
al., 1993). The Greenland ice records have higher d18O
during this interval than that corresponding to the two
older tusks from the Taimyr Peninsula (Dansgaard et al.,
1993); thus 210 derives from a climate that was somewhat
warmer globally. In north central Siberia, this interval
(Middle Weichselian I; Sher et al., 2005) was also
characterized by warm steppe-tundra and summers that
were cooler than during the Middle Weichselian II interval
but still warmer than present. Although the range for 210
(20.9–18.1%) completely overlaps with that from the older
288, the mean value for 210 (19.370.74) is about 1%
higher than that for 288, which is consistent with the higher
d18O values in the Greenland ice cores during interstadial 8.
Jarkov is the youngest tusk from the Taimyr Peninsula and
dates to before the last glacial maximum during MIS 2. The
calibrated age of Jarkov corresponds to the lowest d18O
values of stadial 3 in the Greenland ice sheet (Dansgaard
et al., 1993). This interval is the Sartanian stadial (Late
Weichselian) in north-central Siberia, which is characterized by cold tundra-steppe and cold, dry summers (Sher
et al., 2005). Mean d18O for Jarkov (15.371.29%) is 3–4%
lower than the values for the other tusks from the Taimyr
Peninsula, which is consistent with colder conditions
globally recorded in the Greenland ice sheet. The d18O
profile for Jarkov is also more variable than the other
tusks.
None of these tusks exhibit coherent patterns of seasonal
variation in either second-order increment or d18O profiles
such as have been seen in Mammuthus from midcontinental North America (Koch et al., 1998; Fisher
et al., 2003). It is beyond the scope of this paper to address
evidence and arguments for multiannual migrations by
Siberian mammoths (Fisher and Beld, 2002), but such
behavior could be a confounding factor for both growth
increment and d18O profiles from the Taimyr tusks.
However, growth increments clearly indicate that the last
two years of life in 288 (Fig. 1) do not exhibit strong
seasonality in either tusk growth or d18O values. The
results from the three Taimyr series are climatically
coherent: the highest d18O values are for a tusk from an
interstadial during MIS 3, the intermediate values are for a
tusk from a stadial during MIS 3, and the lowest values are
for a tusk from MIS 2 just before the Last Glacial
Maximum. Warmer intervals thus appear to have been
characterized by higher d18Omw as expected, which led to
higher mammoth d18Oap.
5.2. Chukotka
Results for the two tusks from Chukotka (ZCHM-18
and -16; Fig. 2) have quite similar growth increment and
d18O profiles. The radiocarbon age for the older of the two
Chukotka tusks, ZCHM-18, is beyond the range of the
calibration curve of Fairbanks et al. (2005). The younger
tusk, ZCHM-16, has a calibrated age that falls between the
peak of Greenland interstadial 14 and stadial 14. ZCHM16 has higher mean d18Oap (19.170.74%) and a lower
range (3.4%) than the older ZCHM-18 (17.671.35 and
7.8%, respectively). Both tusks correspond to the early part
of the Middle Weichselian I phase of MIS 3 in northcentral Siberia, characterized by warm steppe-tundra,
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161
Fig. 2. Growth increment and d18O profiles for (A) ZCHM-18 and (B) ZCHM-16 from Chukotka. Vertical lines with arrows indicate positions of
winter–spring boundaries with the number of second-order increments indicated. In each plot, earlier portions of life are to the left and time of death is
marked by the dagger at the sample from the pulp cavity surface.
summers that were dry and warmer than today, and
winters that were colder than today (Sher et al., 2005).
Based on the correspondence between mean d18O values of
the Taimyr Peninsula tusks and the conditions recorded by
the Greenland ice sheet discussed above in Section 5.1, we
suspect that ZCHM-18 derives from a cooler interval than
ZCHM-16, but this is hard to assess given the old
radiocarbon age of ZCHM-18. Additionally, we cannot
determine whether the greater variability in ZCHM-18 is
characteristic of a different climatic interval in easternmost
Siberia or if it is only due to normal interannual variability.
Unlike the Taimyr tusks, the growth increment and d18O
profiles from both Chukotka tusks exhibit regular seasonal
variations. Surprisingly, in most years in both tusks, the
highest d18O values occur in late winter, just before the
winter–spring boundary. In North American Mammuthus
tusks with seasonal variations in d18O, high values
correspond to summer based on second-order growth
increments (Koch et al., 1998; Fisher et al., 2003). We
discuss possible explanations for the high winter d18O
values in Section 6.
5.3. Wrangel Island
The five Wrangel Island tusks are all from the middle
Holocene, with three of them clustered in age around 6.5 ka
and two of them close to 4.3 ka (Table 1). Variation in
mean d18O value among the five tusks does not appear to
correlate with age as the highest mean (21.470.51%) is for
tusk 34M, dated to 6.2 ka, and the lowest mean
(19.470.88%) is for the oldest tusk we analyzed from
Wrangel Island, 29M, which is dated to 6.6 ka. In general,
mean d18O values among the Wrangel tusks are similar,
and the ranges of values from all five tusks overlap.
Growth increment profiles (Fig. 3) are generally seasonal in
character with highest growth rates during summer, but a
mid-year drop in growth rate appears to be common.
Oxygen isotope profiles from Wrangel Island appear to fall
into two modalities. Three of the tusks exhibit d18O profiles
like that in 9M, which has a somewhat irregular pattern
that might be like the typical North American pattern with
high values during summer and early fall but occasional
unusually low values that make a strictly seasonal pattern
hard to discern. 29M exhibits a more regular seasonal d18O
profile (with a superimposed trend toward higher values
over the last couple years of life) but with the same inverse
seasonal pattern of higher winter d18O values exhibited by
the two tusks from Chukotka. The Holocene global
hydrologic cycle was isotopically lighter than the late
Pleistocene cycle due to the contribution of 16O from
melted ice sheets. To be comparable to the Pleistocene
data, values for the Wrangel Island tusks should be
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Fig. 3. Growth increment and d18O profiles for (A) 9M and (B) 29M from Wrangel Island. Vertical lines with arrows indicate positions of winter–spring
boundaries with the number of second-order increments indicated. In each plot, earlier portions of life are to the left and time of death is marked by the
dagger at the sample from the pulp cavity surface.
adjusted higher by about 1% to account for the difference
in ice volume from the late Pleistocene to the Holocene.
6. Discussion and conclusions
Our results do not suggest that in years sampled any of
the animals migrated long distances latitudinally. Given
that all years sampled in these animals had fewer than 52
second-order increments, we suspect that all animals were
resident at high latitude during these years and that
latitudinal variation in the d18O of meteoric water is not
a prominent factor in the data presented here. Full series of
samples from entire life histories might reveal longer-term
variations in isotopic composition that reflect patterns of
interannual latitudinal migration.
Three aspects of our results are particularly striking and
potentially bear on the role of climate change in the
extinction of M. primigenius during the late Pleistocene on
the mainland and the middle Holocene on Wrangel Island.
First, the spatial gradient in late Pleistocene mammoth
d18O values across Siberia is remarkably similar to the
spatial gradient in d18Omw values today (Fig. 4; Kurita
et al., 2004). Considering only the higher latitude (4601 N)
SNIP stations (which have lower d18O values than the
lower latitude stations due to the latitudinal gradient in
temperature), the longitudinal gradient in mean annual
d18Omw values is 0.064%/degree of longitude and the
decrease in d18Omw from west (northern Ukraine/Russia)
to east (northeastern Yakutia) is about 8%. The regression
of d18Omw values as the dependent variable on longitude as
the independent variable is statistically significant
(p ¼ 0.03) even though the number of stations (6) is small.
If all stations, not only those at higher latitude, are
included (n ¼ 13), the regression is not significant
(p ¼ 0.08) and the gradient is slightly less (0.048/1
longitude). In either case, the decrease in d18Omw with
longitude is due primarily to the continental effect, as
discussed in Section 3. Although the easternmost higher
latitude SNIP station (Ayon) has the most negative d18O
values, they are actually less negative than expected from
the Rayleigh distillation model due to the influence of
moisture derived from nearby marine sources (northern
Pacific and Arctic Oceans; Kurita et al., 2004).
Without accounting for variations in age among the
samples from each region, the longitudinal gradient in
mammoth d18O values from sites in the Ukraine and
European Russia to Yakutia is evident, as is the deviation
to higher values of the two mammoths from Chukotka.
Genoni et al. (1998) published d18O values of mammoth
apatite phosphate, which is systematically lower than
corresponding apatite carbonate values by about 8.7%
(Bryant et al., 1996; Iacumin et al., 1996). We used least
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Fig. 4. Spatial variation in d18O values of (A) Siberian mammoths and (B)
modern meteoric water in Siberia. Mammoth data from Ukraine/Russia
and Yakutia from Genoni et al. (1998) are from PO4 and converted to
equivalent CO3 values using data from Bryant et al. (1996) and Iacumin et
al. (1996). Approximate longitude of samples from each region is
indicated. Meteoric water data from Kurita et al. (2004).
squares linear regression of paired phosphate and carbonate d18O values of modern mammals in Bryant et al.
(1996) and Iacumin et al. (1996) to transform the
phosphate d18O data in Genoni et al. (1998) into the
equivalent carbonate d18O values; the 95% confidence
interval for the slope of the regression (70.03) is much
smaller than the range of variation in the mammoth data
discussed here. The mean value for the Ukraine/Russian
data from Genoni et al. (1998) is 21.170.63% and the
range in the data (2.4%), despite ages for sites that range
from 24.3 to 14.3 ka, is comparable to the variation within
each of our tusk series. The mean d18O for the four Taimyr
tusks is 17.7%. The mean d18O for the three Yakutian
samples from Genoni et al. (1998) is 14.7%, and, again
despite the age range in the samples (10 to 440 ka), the
range among the three values is less than in all of the
individual tusk series. The samples from these three regions
span approximately 1001 of longitude, so the gradient
across them is 0.064%/degree, almost exactly the same as
the gradient in modern d18Omw values. This result suggests
that the relationship between mammoth d18Oap values and
local meteoric water has a slope close to 1.0, as is the case
for modern elephants (0.94; Ayliffe et al., 1992). The
positive deviation of the mean values from Chukotka
relative to the trend for the more westerly sites is also
similar to the modern meteoric water pattern. Thus, our
results suggest that at the continental scale, the pattern of
163
moisture transport across Eurasia and the intensity of the
continental effect on meteoric water isotopic composition
during the late Pleistocene was probably similar to modern
patterns. As our data set expands with analyses of
additional dated tusks, we should be able to examine
how the gradient varied through time with greater
resolution.
Second, the pattern of seasonality of d18O values in
Chukotka during MIS 3 was similar to the pattern on
Wrangel Island during at least some parts of the middle
Holocene. We attribute the unexpected pattern of higher
d18O values during winter to two factors. Today, winter
precipitation in easternmost Siberia includes a large
component of moisture derived from the nearby northern
Pacific and/or the Arctic Ocean that would not have
become depleted in 18O through rain-out and thus would
have higher d18O values than expected based on air
temperature and the Rayleigh distillation model for
Atlantic-derived moisture. However, winter precipitation
in Ayon in western Chukotka still has lower d18O values
than summer precipitation. A second factor is the amount
of recycled moisture included in summer precipitation,
which has a negative correlation with d18Omw of summer
precipitation today (Kurita et al., 2004). A larger
contribution of winter snow melt to the recycled water,
as might be expected during MIS 3 and even episodically at
times during the Holocene on Wrangel Island, and warmer,
drier summers with enhanced surface evaporation (which
would preferentially move 16O into vapor) would both
yield recycled moisture with a lower d18O value. Given that
summer d18Omw values would be low because of the
continental effect anyway, it is possible that greater winter
snow melt and increased surface evaporation could
actually yield summer d18Omw values that were lower than
winter values (hence the seasonality patterns in ZCHM-18
and -16 and 29M) despite higher air temperatures than in
winter. The similarity between the seasonality patterns for
some of the tusks from easternmost Siberia also suggests
some degree of climatic continuity in the region from the
late Pleistocene to the middle Holocene.
Finally, the temporal gradients in mean d18O values in
Taimyr and in easternmost Siberia, which should be a
proxy for changes in mean annual temperature in each
region, are similar over different climatic intervals. Considering only mean d18Oap values, the temporal gradient in
Taimyr from interstadial conditions during MIS 3 (210,
19.3%) and conditions close to a stadial in MIS 2 prior to
the glacial maximum (Jarkov, 15.3%) is 4%. Correcting for
the ice volume effect on the Wrangel tusks, the temporal
gradient in easternmost Siberia from the lowest mean d18O
for MIS 3 (ZCHM-18, 17.6%) to the highest value for
Wrangel Island (34M, 21.4% measured, 22.4% adjusted) is
4.8%. If we use the mean values for all of the individual
samples from both Chukotka tusks (18.4%) and all five
Wrangel tusks (20.7%), the difference is only 2.3%. From
these data, it appears that the degree of climate change
recorded by tusks in easternmost Siberia from the
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interstadial conditions of MIS 3/Middle Weichselian to the
middle Holocene may have been about the same as the
degree of climate change from MIS 3/Middle Weichselian
to the last glacial maximum in the Taimyr Peninsula.
We propose that climate alone was not a driving factor
behind the extinction of M. primigenius in Eurasia during
either the late Pleistocene or the late Holocene. Our results
obviously do not rule out floral changes in response to
climate change as a cause, nor human hunting in
combination with range and population size reductions.
Of course, survival of M. primigenius on Wrangel Island
across the glacial–interglacial transition at the end of the
Pleistocene and into the middle Holocene by itself implies
that climate change and absolutely warmer Holocene
conditions in eastern Siberia were not sufficient to cause
extinction of mammoths. We will need to test these
patterns with more data from tusks from Siberia and
augment our interpretations with additional paleobiological information from carbon and nitrogen isotope profiles
from these and other tusks, but observations reported here
already raise issues that must be addressed by climatedriven models of the extinction process.
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