Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
Contents lists available at SciVerse ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology
journal homepage: www.elsevier.com/locate/palaeo
Paleoecology of late Pleistocene–Holocene faunas of eastern and central Wyoming,
USA, with implications for LGM climate models
Matthew J. Kohn a,⁎, Moriah P. McKay b
a
b
Department of Geosciences, Boise State University, Boise, ID 83725, United States
Department of Geological Sciences, University of South Carolina, Columbia, SC 29208, United States
a r t i c l e
i n f o
Article history:
Received 7 September 2011
Received in revised form 23 January 2012
Accepted 30 January 2012
Available online 11 February 2012
Keywords:
Pleistocene
Carbon isotopes
Oxygen isotopes
Tooth enamel
Paleoecology
a b s t r a c t
Oxygen and carbon isotope compositions of teeth were measured for a variety of fossil herbivores, omnivores
and carnivores from Natural Trap Cave (NTC) and Little Box Elder Cave (LBEC), central eastern Wyoming,
USA. These sites host some of the best preserved and most abundant late Pleistocene to early Holocene mammal
fossils, and provide key information about ecological and climatic change attending the Pleistocene–Holocene
transition. Average Pleistocene compositions are consistent with C3-dominated diets, but C4 grass consumption
increased in Bison from the late Pleistocene to today. A single Sangamonian Equus tooth also has elevated 13C,
suggesting that C4 biomass increased during interglacials in general. Tooth δ18O values imply local water δ18O
values at NTC of − 15 to − 16‰ during the Last Glacial Maximum (LGM) and − 14‰ today, consistent
with modern regional studies and general circulation models (GCM's) for the LGM. Water δ 18O values at
LBEC were ~−12‰. Although herbivore compositions are consistent with theoretical expectations, carnivores exhibit lower δ 13C and higher δ 18O values relative to herbivores than anticipated. These discrepancies
could reflect poorly understood carnivore physiologies or diets, and emphasize the need for further investigation of isotope systematics in carnivores. Isotope zoning in several herbivore teeth shows negative correlations between carbon and oxygen isotopes: high and low δ 18O values representing summer and winter
seasons occur with low and high δ 13C values respectively. This trend could indicate seasonally changing
diets, e.g. consumption of drier foods or conifers during the winter, or burning of stored fat during the winter. Increasing δ 18O values from the Pleistocene to Holocene in water-dependent taxa are consistent with an
increasing proportion of summer moisture derived from the Gulf of Mexico, as predicted by isotopeenabled GCM's. Mean annual precipitation during the late Pleistocene is estimated at ≤ 350 mm/yr, similar
to modern day (c. 200 mm/yr), indicating that dry conditions have prevailed for the last 25 ka in Wyoming.
A revised analytical expression for C4 plant abundance in the western US is proposed that accounts for climate variables and pCO2. Combination of this expression with the climate predictions of the PMIP2 ensemble average GCM explains LGM C4 plant abundances at NTC, southern Texas, and Florida. Changes to C4
plant abundances may provide sensitive tests of GCM accuracies.
© 2012 Elsevier B.V. All rights reserved.
1. Introduction
Characterizing past ecologies and climates in comparison to modern
day conditions helps us understand processes of climate change and
critically evaluate climate models. Late Pleistocene fossils at Natural
Trap Cave (NTC) and Little Box Elder Cave (LBEC), Wyoming (Fig. 1),
provide an unusual opportunity to compare Last Glacial Maximum
(LGM) and modern conditions, and to explore the Pleistocene–Holocene
transition. This transition is important for several reasons. Documented
isotopic and climatic changes are used to validate the accuracy of general circulation models that incorporate stable isotopes (e.g., Joussaume
and Jouzel, 1993; Hoffmann et al., 2000; Jouzel et al., 2000; Risi et al.,
⁎ Corresponding author.
E-mail address: [email protected] (M.J. Kohn).
0031-0182/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2012.01.037
2010) or that are used to predict future climate change (e.g.,
Joussaume and Taylor, 1995; Braconnot et al., 2007; Meehl et al.,
2007). The isotope compositions of diverse faunas prior to the late Pleistocene megafaunal extinction also allow investigation of niche partitioning and diet selectivity in anthropogenically undisturbed
ecosystems, as well as floral changes attending glacial–interglacial cycles (e.g., Koch et al., 1998; Coltrain et al., 2004; Kohn et al., 2005;
Palmqvist et al., 2008). Unlike many faunal sites, an abundance of
canid (“dog”), felid (“cat”), and ursid (“bear”) fossils, in addition to numerous ungulates, further allows comparisons among carnivores, omnivores, and herbivores for understanding predator–prey relations,
effects of trophic level on isotope compositions, and physiological or dietary causes of isotopic outliers.
In this study, we report stable carbon and oxygen isotope compositions of teeth from a diverse suite of animals recovered from these
two caves to explore a series of interrelated ecological, physiological
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
110W
100W
90W
80W
43
TR
H
NTC
40N
LBEC
30N
HG
K04
H06
HM
K/F
Fig. 1. Outline of conterminous United States, Wyoming, and areas studied by Koch et al. (1998) and Feranec (2004b; “K/F”), and Koch et al. (2004; “K04”); dot shows study area of
Huang et al. (2006; “H06”). Sample localities: NTC = Natural Trap Cave and LBEC = Little Box Elder Cave. Topographically high areas in Wyoming are outlined. Holocene sites are: TR
(Tongue River; Melton and Davis, 1999), H (Hawken; Lovvorn et al., 2001), HM (Hudson-Meng; Gadbury et al., 2000; Larson et al., 2001), and HG (Hell Gap; CARD, 2011).
and climatic questions. These questions include: (1) How did late
Pleistocene environments differ from the present, particularly with
respect to C4 plant abundances and water compositions? (2) Relative
to herbivores, are theoretical models of carnivore compositions accurate, and are carnivore–herbivore isotopic offsets consistent with
other empirical measurements? (3) What possibilities explain isotopically anomalous taxa relative to better-studied and more typical
species? (4) What seasonal changes to diet or climate are inferable
from intra-tooth isotope zoning? (5) What changes to mean annual
precipitation (MAP) and δ18O values occurred across the Pleistocene–
Holocene transition, and how do they compare with GCM predictions?
(6) How do estimates of C4 abundance trends, as derived from δ13C
values of herbivore teeth, compare with predictions linked to GCM's?
2. Stable isotopes of teeth
Teeth consist mineralogically of hydroxyapatite with major substitution of CO3 for PO4 and OH groups. In this study we analyzed the
CO3 component for δ 13C and δ 18O values. For reviews of stable isotopes in teeth, see Koch (1998, 2007), MacFadden (2000), Kohn and
Cerling (2002) and Kohn and Dettman (2007). Oxygen isotopes in
herbivore tooth enamel correlate with local water compositions
(Kohn, 1996), but drought-tolerant species exhibit additional negative correlations with relative humidity (Ayliffe and Chivas, 1990;
Luz et al., 1990). Oxygen isotopes in carnivores are assumed to correlate with local water as well (Kohn, 1996), but the modern data set is
too small to verify this assumption generally, and isotope data from
felid hair suggests poor correlations (Pietsch et al., 2011). Carbon isotopes correlate with diet. In mixed C3–C4 ecosystems, grazers exhibit
elevated δ 13C values compared to browsers in proportion to the ratio
of C4 to C3 consumed. δ 13C values of C3 plants and the animals that
consume them increase with decreasing MAP (e.g., Farquhar et al.,
1989), and in principle the δ 13C value of tooth enamel in C3 ecosystems can be used to infer past MAP (Kohn, 2010).
Teeth mineralize progressively from the tip or occlusal surface toward the root. Because local water compositions vary seasonally
(lower in winter and higher in summer), oxygen isotope zoning
both provides a measure of climate seasonality and indicates when
different portions of a tooth mineralized. When paired with carbon
isotope analysis, changes in diet can be identified and correlated
with season.
In principle, an ontogenetic shift from nursing to an adult diet can
change isotope compositions both within teeth that mineralize over a
significant period as well as among teeth that mineralize at different
times. Although this effect is well documented for human oxygen
and carbon isotope compositions (Wright and Schwarcz, 1998), results for other animals are scattered and inconclusive. Some data for
mammoths suggest that neonate tooth enamel has lower δ 13C and
higher δ 18O values than adults (Metcalfe et al., 2010). Other data
from 11 modern mammal species, however, show no δ 13C differences
in the plasma of nursing juveniles and their mothers (Jenkins et al.,
2001). Oxygen isotope compositions of teeth that formed during
and after nursing are not predicted to be different (Kohn et al.,
1998), and studies of large wild herbivores have failed to identify a
clear oxygen isotope effect (Kohn et al., 1998; Gadbury et al., 2000;
Murphy et al., 2007; Forbes et al., 2010).
Although the timing of tooth formation and mineralization has
been discussed extensively for herbivores, carnivores have received
less attention. We have found little direct information on rates of
tooth enamel mineralization in modern carnivores, but diverse
sources document the timing of weaning and of the initial appearance
or eruption of different teeth in the jaw (Saunders, 1964; Slaughter et
al., 1974; Smuts et al., 1978; Mazak, 1981; Currier, 1983; Gittleman,
1986; Pusey and Packer, 1994; Biknevicius, 1996; Hillson, 1996;
Miles and Grigson, 2003; Strömquist et al., 2009; see Supplemental
file). In general, relative to birth, the first permanent cheek teeth in
felids and canids erupt 2 times later than the timing of weaning. For
example, weaning in Vulpes occurs on average at 1.8 months, whereas
eruption of most cheek teeth occurs at 4–6 months. In Panthera pardus,
weaning occurs on average at 4.6 months, whereas canines, molars, and
premolars do not erupt until 8–10 months. Canine growth in Panthera
leo is well studied. Whereas weaning occurs at 7 months, mineralization of the canine does not initiate until 9–11 months, initial eruption
occurs soon after (11–15 months), and final mineralization concludes
by 28–36 months. Stable isotope zoning in Smilodon canines implies
similarly lengthy durations of mineralization (Feranec, 2004a). Considering that meat consumption commences well prior to weaning, the
isotopic effects of milk consumption on cheek teeth and canines in canids and felids should be negligible. Consequently, we emphasized
their analysis in this study. In contrast, weaning in Ursus arctos
at ~2 years postdates initial eruption of canines (8 months) and cheek
teeth (12–24 months), although canine growth can continue past
50 months. Thus, in principle milk consumption could affect ursid isotope compositions.
3. Specimens and methods
3.1. Specimens and research sites
Specimens were provided by the University of Kansas Museum of
Natural History and the University of Colorado at Boulder. In our discussion and interpretations, we emphasize NTC more than LBEC because of the larger number of specimens and generally better
chronology and stratigraphy. Note that county-wide grass surveys
in Wyoming indicate that the C4 photosynthetic pathway comprises
c. one-quarter of generic and one-sixth of species diversity in Big
Horn County (NTC) and c. one-third of generic and one-quarter of
species diversity in Converse County (LBEC) (USDA and NRCS,
44
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
2011). C4 biomass has not been measured directly in either area, but
regional correlations and data compilations (Paruelo and Lauenroth,
1996) suggest at most 20% C4 biomass at both NTC and LBEC.
Natural Trap Cave (Fig. 1) is a karst feature within the Mississippian Madison Formation on the western slope of the Big Horn Mountains, near Lovell, Wyoming. At ~ 1400 m elevation, local topography
obscures the sinkhole cave's opening to a ~25 m drop. Excavations
of NTC from 1974 to 1985 recovered over 40,000 specimens, or ~5%
of the deposit (Wang and Martin, 1993). Taxa analyzed included numerous herbivores (Bootherium bombifrons, Bison sp., Antilocapra
americana, Ovis canadensis catclawensis, Camelops sp., Equus sp.,
Mammuthus sp., Bos taurus, Odocoileus sp., and two unidentified artiodactyls), several carnivores (Canis lupus, Gulo gulo, Miracinonyx trumani,
and Panthera atrox), and several omnivores (Vulpes vulpes, Canis latrans,
Arctodus simus, and U. arctos).
Ages for NTC are based on 14C measurements on bone collagen
(Chomko and Gilbert, 1987; Walker, 1987; CARD, 2011) and converted to YBP using IntCal09 (Reimer et al., 2009). Most ages range
from c. 26 ka to 11 ka. Several teeth from the Sangamon interglacial,
dated at ~110 ka (Chorn et al., 1988), were also analyzed. Pleistocene
data were augmented with isotope measurements of a historical B.
taurus tooth, several published Holocene bone collagen analyses
(Bison bison; Haynes, 1968; Melton and Davis, 1999; Gadbury et al.,
2000; Larson et al., 2001; Lovvorn et al., 2001), and modern measurements of A. americana teeth (Fenner and Frost, 2009). Many specimens are correlated stratigraphically, permitting direct comparisons
among taxa, although in some cases their ages are only bracketed
with 14C dates, leading to relatively large absolute uncertainties.
Little Box Elder Cave (Fig. 1) is located ~30 km west of Douglas,
Wyoming, at ~ 1675 m elevation; it formed either by solution of the
Mississippian Amsden Formation or by lateral cutting of a nearby
creek. Excavations between 1949 and 1963 recovered over 15,000
specimens, or approximately two-thirds of the deposit (Anderson,
1968). Taxa analyzed include herbivores (Equus sp., B. bison, Cervus
elephus, Odocoileus hemionus, O. canadensis, and Oreamnos sp.), carnivores (Lynx rufus, Puma concolor, C. lupus, and Taxidea taxus) and omnivores (V. vulpes, A. simus, and U. arctos). Little Box Elder Cave is
commonly assumed to span the Pleistocene–Holocene transition
(Kurten and Anderson, 1980). 14C ages range from latest Pleistocene
to early Holocene (Walker, 1987).
3.2. Analytical methods
We used the method of Kohn et al. (2005) for sampling and analysis of enamel. This involves cutting a strip of enamel lengthwise
along each tooth, subsampling every 1–2 mm, cleaning subsamples
of adhering dentine, and preparing and analyzing the resulting purified enamel using the method of Koch et al. (1997). This latter method involves grinding the enamel to a fine powder, pretreating in H2O2
and an acetic acid–Ca-acetate buffer, and analyzing in an automated
carbonate extraction device, on-line with a mass spectrometer. For
this study, analyses were collected with a VG Optima mass spectrometer at the University of South Carolina. Three to five aliquots of
NIST120c were prepared and analyzed with each batch of 20–25 unknowns. Six to seven analyses of NBS-19 calcite were also collected to
verify mass spectrometer operation and reference gas calibrations.
Data are reported in permil relative to V-SMOW for oxygen, and VPDB for carbon (Tables 1–2; Supplemental files). Means for NIST120c were δ 18O = 28.8 ± 0.8‰ (2σ) and δ 13C = − 6.4 ± 0.4‰ (2σ).
Errors include intra-run and day-to-day variations in sample preparation and analysis. Comparisons of mean values were assessed statistically using Mann–Whitney non-parametric tests; t-tests yield similar
Table 1
Average compositions of taxa at Natural Trap Cave and Little Box Elder Cave, Wyoming, USA.
Taxon
n
δ13C
(‰)
2σ
(‰)
δ18O
(‰)
2σ
(‰)
Natural Trap Cave
Bootherium
Bison
Antilocapra
Camelops
Ovis
Equus
Mammuthus
Cervid
Bos
Odocoileus
C. lupus
Gulo
Miracinonyx
Panthera
Vulpes
Arctodus
C. latrans
Ursus
7/49
7/46
6/30
3/8
8/48
21/123
5/28
1/7
1/8
1/3
8/24
3/6
5/15
2/5
3/9
3/6
1/3
1/3
− 10.0
− 8.3
− 10.0
− 9.0
− 9.2
− 10.2
− 9.3
− 9.9
− 8.5
− 13.4
− 11.6
− 12.7
− 11.2
− 11.9
− 12.3
− 13.1
− 7.9
− 8.2
0.67
1.33
1.32
1.06
1.01
1.58
1.00
0.99
1.92
0.61
1.0
1.5
2.9
0.6
1.3
2.3
0.4
0.5
17.0
18.3
19.7
16.5
19.0
17.5
18.0
17.5
18.8
27.3
22.2
21.6
21.5
21.9
26.1
20.1
30.3
18.9
3.28
4.73
5.92
2.66
4.72
3.26
2.09
3.08
2.61
0.90
1.1
5.4
3.9
2.2
1.7
1.6
1.6
3.8
6/26
4/17
2/6
5/18
2/8
2/4
3/5
2/3
3/8
1/2
3/8
1/3
3/5
− 11.5
− 8.1
− 10.9
− 10.3
− 9.1
− 10.3
− 13.9
− 13.3
− 10.9
− 9.4
− 15.7
− 14.9
− 11.8
1.5
3.3
1.4
2.4
0.8
1.0
1.5
1.9
3.0
2.0
1.1
0.2
1.6
21.6
19.8
22.9
20.5
21.4
21.7
27.0
26.6
24.1
23.7
23.5
22.8
27.5
5.1
5.2
3.9
4.6
4.2
5.4
3.8
1.3
4.2
2.0
1.0
0.5
3.2
Little Box Elder Cave
Equus
Bison
Odocoileus
Ovis
Oreamnos
Cervus
Lynx
Taxidea
C. lupus
Felis
Ursus
Arctodus
Vulpes
Note: n = number of teeth sampled/total number of analyses.
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
45
Table 2
Secular changes to tooth enamel compositions for select taxa at Natural Trap Cave, Wyoming, USA.
Age (a)
2σ (a)
n
δ13C
(‰)
2s.e.
(‰)
δ18O
(‰)
2s.e.
(‰)
Antilocapra
25,800
21,350
17,800
16,300
10a
2200
750
1700
2400
5
4
6
12
8
42
− 10.50
− 9.83
− 9.93
− 9.86
− 10.99
0.98
0.43
0.36
0.44
0.14
20.47
19.83
19.72
19.14
23.88
4.43
2.14
1.34
2.63
0.44
Bison/Bos
23,650
21,350
18,100
16,300
15,400
5000
10000b
200
100a
7280a
100a
10000a
10900a
4350
750
6050
2400
2300
5000
5000
200
100
150
100
300
200
6
5
5
6
9
6
17
8
65
1
59
1
1
− 9.53
− 9.01
− 8.59
− 7.83
− 8.48
− 7.72
− 8.1
− 8.54
− 5.52
− 6.0
− 6.58
− 6.42
− 9.4
0.33
0.47
0.15
0.20
0.24
0.69
0.8
0.34
0.83
1.30
0.25
15.81
20.15
15.59
19.32
17.87
18.66
0.83
1.92
0.85
2.61
1.04
1.71
18.76
0.46
22.1
0.59
Equus
110,000
25,800
24,250
23,650
22,700
21,350
17,800
16,300
15,400
14,300
12,800
10,000
2200
700
4350
3150
750
1700
2400
2300
2600
650
7
7
7
20
3
16
13
7
12
8
7
− 7.28
− 10.96
− 11.23
− 9.83
− 10.37
− 9.81
− 10.86
− 9.37
− 10.78
− 9.61
− 9.82
1.05
0.46
0.20
0.26
0.30
0.25
0.38
0.28
0.44
0.11
0.24
14.28
16.15
16.96
17.05
17.33
16.72
18.00
16.96
18.92
18.34
18.39
0.83
0.26
0.23
0.43
0.69
0.82
0.49
0.32
1.90
0.64
0.30
Ovis
110,000
21,350
21,250
17,800
15,400
10000b
10,000
750
3800
1700
2300
5000
7
9
8
5
12
18
− 10.01
− 8.99
− 9.83
− 8.81
− 9.31
− 10.30
0.08
0.11
0.18
0.19
0.20
0.50
20.56
17.65
20.00
18.93
19.79
1.98
1.46
0.86
2.17
1.25
a
b
Published data from Melton and Davis (1999), Gadbury et al. (2000), Larson et al. (2001), Lovvorn et al. (2001), and CARD (2011).
Carbon isotope data from LBEC (δ18O not included because of systematic geographic differences).
results. Select results are presented here; comprehensive interspecies
and time-slice comparisons are provided in McKay (2008). Mean
values across taxa (e.g., all NTC LGM herbivores, all large LBEC carnivores, etc.) were calculated by weighting according to measured variation of individual taxa; corresponding errors were estimated from the
weighted standard deviation of observations about the mean (cf.
Kohn and Spear, 1991a).
3.3. Modeling
Oxygen isotope modeling used the approach of Kohn (1996),
modifying key oxygen fluxes and input/output compositions to explore compositional sensitivities (Table 3).
Mean annual precipitation (MAP) was estimated based on C3
plant δ 13C using the approach of Kohn (2010). Because plant compositions have not been measured, we instead use the isotope compositions of tooth enamel from herbivores that consumed C3 plants only,
correcting for the known fractionation between diet and tooth enamel
(Passey et al., 2005) and changes to δ13Catm. We adopt an average
δ13Catm value of −7.0 during the late Pleistocene, −6.5 during the
pre-industrial Holocene, and −8.0 for today (Smith et al., 1999). Relative to modern δ13Catm = −8.0, average δ13C values of deciduous C3 angiosperms are lower than −24.3‰ (Kohn, 2010). Correcting for
fractionations between diet and tooth enamel (Passey et al., 2005:
14.5‰ for artiodactyls and 14‰ for other herbivores), we adopt an isotopic cutoff for C3 consumption by artiodactyls (all herbivores at LBEC
and NTC except Equus) of −9.8‰ today, −8.8‰ during the late Pleistocene, and −8.3 during the pre-industrial Holocene. Higher values imply
consumption of other 13C-enriched foods, including CAM and C4 plants.
Isotopic cutoffs for Equus are 0.5‰ lower. Note that changes to pCO2 alone
are not thought to influence terrestrial C3 plant δ13C (Arens et al., 2000).
Estimating MAP from δ 13C values requires rewriting the relationship between modern plant δ 13C (referenced to δ 13Catm = − 8.0‰)
and MAP to solve for MAP as a function of δ 13C, elevation (in meters)
and latitude (absolute value in °):
"
MAP ¼ 10ˆ
#
13
δ C þ 10:29−0:000194 elev þ 0:0124 Absðlat Þ
−300:
−5:61
ð1Þ
In addition, we evaluate the uncertainty in calculated MAP according to the standard error propagation equation (cf. Kohn and Spear,
1991b):
2
σ MAP ¼ ∑ ∑
j
i
!
∂MAP
∂MAP
σ i σ j ρij
∂X i
∂X j
ð2Þ
46
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
Table 3
Models of herbivore and carnivore δ18O.
Model
Drinking H2O
(%, δ18O)
Food H2O
(%, δ18O)
Water econ. index
Dry food δ18O
(‰)
H2O vapor, liquid output
(%)
Model δ18O
(‰)
Standard herbivore
Standard carnivore
Low WEI
High δ18O H2O
High δ18O protein
High vapor output
Maximum carnivore
23,
57,
2,
57,
57,
46,
2,
− 15.0
− 15.0
− 15.0
− 15.0
− 15.0
− 15.0
− 15.0
63, − 9.9
34, − 8.0
78, − 8.0
34, − 3.0
34, − 8.0
43, − 8.0
43, − 3.0
0.25
0.25
0.11
0.25
0.25
0.20
0.11
18.8
− 1.0
− 1.0
4.0
20.0
− 1.0
20.0
34,
52,
41,
52,
52,
57,
57,
17.5
16.7
17.1
18.1
17.0
17.4
20.5
43
25
19
25
25
16
16
Note: δ18O values are in ‰ relative to V-SMOW; water economy index is the ratio of daily water turnover in ml to energy expenditure in KJ; the % vapor and liquid H2O output is
relative to total oxygen (which includes CO2). High vapor output model has reduced fecal water content (50%, rather than 60%) and urine output (15% rather than 25%).
where ∂MAP/∂Xi and ∂MAP/∂Xj are the partial derivatives of Eq. (1)
with respect to the variables Xi and Xj, σi and σj are the uncertainties
in Xi and Xj, and ρij is the correlation coefficient between Xi and Xj.
Correlation coefficients are known from the original linear regression,
and errors can be assumed from reproducibilities or data scatter. Partial derivatives, however, are most easily estimated numerically
(Roddick, 1987). In this approach, we perturb each parameter in
Eq. (1) by a small amount (Δi, typically ~ 1%), and determine a new
value for MAP, here denoted MAP*. The partial derivative of Eq. (1)
with respect to the parameter Xi (∂MAP/∂Xi) is then simply (MAP*
− MAP) / Δi. We then successively multiply partial derivatives, errors
and correlation coefficients, sum over all parameters and errors, and
take the square root. In general, the magnitude of each error increases
with increasing MAP, increasing elevation, and decreasing latitude,
but the 2σ uncertainty is approximately 50% of MAP above
~ 500 mm/yr, and never falls below ~±120 mm/yr (Fig. 2).
4. Results
4.1. Mean isotope compositions
Average δ 18O values at NTC (Fig. 3) are systematically ~ 3‰ lower
than at LBEC (Fig. 4; p b 0.001), but δ 13C values generally overlap, and
relative isotopic differences among groups are consistent at the two
sites. For example, relative to Pleistocene herbivores, Pleistocene carnivores consistently show elevated δ 18O, c. 3–4‰, both at NTC (Fig. 3;
p b 0.001) and LBEC (Fig. 4; p b 0.001). Some studies have shown similar
results (Bösl et al., 2006; Garcia Garcia et al., 2009; Feranec et al., 2010),
but others show overlapping carnivore–herbivore compositions (Kohn
et al., 2005; Palmqvist et al, 2008). Pleistocene carnivore δ13C values
are consistently lower than herbivores at NTC by ~2‰ (pb 0.001;
2.3‰ for all carnivores, and 2.2‰ considering large carnivores only).
This difference is slightly larger than anticipated from careful carnivore–
herbivore comparisons of bone (Clementz et al., 2009). Large carnivores
at LBEC (C. lupus and Felis) have c. 3‰ higher δ13C values than small carnivores (Lynx and Taxidea; p b 0.001), with a near-zero offset between
large carnivores and herbivores (p= 0.96). Carnivore–herbivore comparisons at LBEC may be compromised by uncertainty in whether individual carnivore specimens reflect late Pleistocene or Holocene
ecosystems. Collagen isotopic compositions at NTC (McNulty et al.,
2002) and measured isotopic offsets between bioapatite and collagen
(Clementz et al., 2009) imply bioapatite δ 13C values of c. −10 to
−11.5‰ for herbivores and −13 to −15‰ for carnivores, 1–2‰
lower than reported here. The small number of collagen analyses and
wide spread of ages does not allow close comparison of these different
datasets, however, except to note that relative isotopic spacings among
taxa are preserved regardless of tissue. Tooth enamel analyses from 6
large herbivore teeth (Higgins and MacFadden, 2009) overlap ours.
Bears exhibit δ 18O values intermediate between carnivores and herbivores (Figs. 3–4). Arctodus shows distinctly lower δ13C values, as does
32.5
Natural Trap Cave
30.0
Canis latrans
(Hol.)
Odocoileus
(Hol.)
Elevation = 1500m
Latitude = 45°
2500
MAP (mm/yr)
2000
1500
δ18O (‰, V-SMOW)
27.5
3000
25.0
22.5
Panthera Canis lupus
Gulo
Miracinonyx
20.0
Arctodus
(pre-Hol)
Antilocapra
Equus
Bootherium
15.0
Mammuthus
12.5
500
Ovis
Ursus (Hol.)
17.5
Equivalent
modern C3
Composition
Herbivore
Wtd Mean
Cervid
±2σ
1000
Carnivore
Wtd Mean
Vulpes
(pre-Hol)
-16.0
-14.0
-12.0
-10.0
Bos (Hol.)
Bison
Camelops
-8.0
-6.0
δ13C (‰, V-PDB)
0
-500
-30
-29
-28
-27
-26
-25
-24
δ13C (‰, V-PDB)
Fig. 2. MAP vs. δ13C at an elevation of 1500 m and latitude of 45°, with ±2σ error envelopes from regression. Error is approximately 50% of MAP, except at low MAP
(c. ±120 mm/yr).
Fig. 3. Summary of data from Natural Trap Cave (see Tables 1–2 and Supplemental file
for data). Data show resource partitioning among taxa, and systematic and large isotopic offset between weighted mean compositions of carnivores vs. herbivores. Carnivore
mean omits bears and small canids (Arctodus, C. latrans, and Vulpes); herbivore mean
omits Holocene taxa (Bos and Odocoileus). The size of the shaded ellipses reflects the
2σ uncertainty in the weighted mean value. A difference in mean δ13C values between
carnivores and herbivores is anticipated from predator–prey isotopic fractionations
(Clementz et al., 2009); oxygen isotope differences are less easily interpreted. “Hol.”
and “pre-Hol.” labels indicate whether outliers are Holocene or pre-Holocene.
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
Ursus at LBEC, but Ursus at NTC has high δ13C values. Besides bears, compositional extremes at NTC (Fig. 3) include C. latrans (high δ18O and
δ13C values), Vulpes (high δ18O values), and Odocoileus (high δ18O and
δ13C values; p ≤ 0.003 for all comparisons). At LBEC, compositional extremes include Vulpes (high δ18O values; p = 0.04) and Bison (low
δ18O, high δ13C values; Fig. 4; p b 0.001).
32.5
Little Box Elder Cave
Carnivore
Wtd Mean
30.0
Vulpes
δ18O (‰, V-SMOW)
27.5
Lynx
Taxidea
25.0
Ursus
Canis
Lupus
Herbivore
Wtd Mean
Odocoileus
47
4.2. Isotope zoning
Felis
22.5
Arctodus
Compositional zoning along large herbivore teeth shows quasisinusoidal variations (Fig. 5), both in δ18O and δ13C. C- and Oisotopes, however, are negatively correlated, i.e. 18O-enriched portions
of a tooth (summer compositions) generally have low δ 13C values,
and 18O-depleted portions (winter compositions) have high δ13C
values. Negative correlations are common among herbivores (Fig. 6), although for most p ≥ 0.1, and not obviously dependent on age (cf. Holocene Bos, post-LGM Bootherium and Antilocapra, and LGM Mammuthus).
Carnivore teeth are generally too small or insufficiently zoned to show
this directly, but one also has a possible negative correlation
(KU26133 Miracinonyx; p = 0.318).
Oreamnos
Equus
20.0
Ovis
Bison
Cervus
17.5
15.0
12.5
-16.0
-14.0
-12.0
-10.0
-8.0
-6.0
δ13C (‰, V-PDB)
Fig. 4. Summary of data from Little Box Elder Cave (see Tables 1–2 and Supplemental
file for data). Data show resource partitioning among taxa, and systematic and large
offset between weighted mean compositions of carnivores vs. herbivores. Carnivore
mean omits bears and small canid (Arctodus, Vulpes, Ursus); herbivore mean includes
all taxa. The size of the shaded ellipses reflects the 2σ uncertainty in the weighted
mean value. A difference in mean δ13C values between carnivores and herbivores is anticipated from predator–prey isotopic fractionations (Clementz et al., 2009); oxygen
isotope differences are less easily interpreted.
4.3. Secular isotope changes
Carbon isotopes (Fig. 7) show steadily increasing δ 13C values for
Bison and Bos from the LGM to the present (p b 0.001). Equus data
from the LGM to Pleistocene–Holocene transition do not statistically
resolve a trend (p = 0.95), but show distinctly higher δ 13C values for
A
-7.0
24.0
Ovis 40577
22.0
-9.0
20.0
δ13C
-10.0
18.0
-11.0
16.0
Occlusal
Surface
Cervical
Margin
Time
-12.0
B
δ18C (‰, V-SMOW)
δ13C (‰, V-PDB)
-8.0
14.0
-7.0
24.0
Bison 36767
22.0
δ13C
20.0
-9.0
-10.0
18.0
δ18O
16.0
-11.0
Occlusal
Surface
-12.0
δ18C (‰, V-SMOW)
δ13C (‰, V-PDB)
-8.0
0
Cervical
Margin
Time
14.0
10
20
30
40
Distance (mm)
Fig. 5. Zoning profiles measured along (A) Bison and (B) Ovis teeth, showing strong and weak zoning in δ18O and δ13C respectively. Note general correspondence between maximum
δ18O and minimum δ13C values. 2σ error bars represent within-run variations on standards.
48
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
LGM to the Holocene (Fig. 8). Ovis and Antilocapra compositions do
not independently confirm this trend (p ≥ 0.10) but are consistent
with it (Fig. 8). C. lupus shows no secular change to δ 18O values
(p > 0.8), although data are restricted to the Pleistocene.
24.0
capra
Antilo
Mi
rac
5. Interpretations
ino
ny
x
20.0
Bo
5.1. Herbivore isotope compositions: water compositions and vegetation
s
18.0
Ce
Bo
16.0
14.0
-11.0
oth
r vi
er
d
ium
-10.0
-9.0
-8.0
-7.0
δ13C (‰, V-PDB)
Fig. 6. δ18O vs. δ13C from individual zoned teeth, showing common negative correlations (cf. Fig. 5); p-values are 0.004 (Bootherium), 0.003 (cervid), 0.056 (Antilocapra),
0.318 (Miracinonyx) and 0.024 (Bos). Lines for Bos, Miracinonyx, cervid and Bootherium
illustrate general consistency among different taxa; line for Antilocapra illustrates different slope. 2σ error bars represent within-run variations on standards. δ13C values
for Miracinonyx have been increased by 2‰ to account for systematic offsets between
carnivores and herbivores.
the Sangamon interglacial (p b 0.001) relative to other Pleistocene
compositions, comparable to Holocene Bison and Bos. Secular changes
for Ovis, C. lupus, and Antilocapra show no consistent major shifts
from the LGM to present (p > 0.05). Statistically, a carbon isotope difference occurs between Sangamon vs. LGM and post-LGM Ovis
(p b 0.02), but because the (essentially homogeneous) Sangamon
tooth composition falls within the range of other Pleistocene teeth,
we do not view the difference as significant. Secular changes in δ 18O
values have been discussed previously (Kohn and McKay, 2010),
and for water dependent taxa (Equus, Bootherium, Mammuthus,
Bison/Bos) show an average 1.8 ± 1.6‰ (2 s.e.) increase from the
0.0
13C
(‰, V-PDB)
-3.0
Equus
Bison, Bos
Ovis
Canis lupus
Antilocapra
30.0
May include
non-C3 plants
(artiodactyl)
-6.0
HG
n
Biso
26.0
H
ctory
traje
HM
Bos
-9.0
-12.0
Applying modern empirical calibrations for Equus, Bovinae, and elephants to data for Equus, Bison, Bootherium, and Mammuthus, Kohn and
McKay (2010) inferred water δ 18O values at NTC of ~−16‰ during the
LGM and ~−14‰ today; the latter value is consistent with regional
compilations of precipitation and local water δ18O values (Coplen and
Kendall, 2000; Friedman, 2000; Dutton et al., 2005). Using the
empirically-derived compositions for NTC, generalized theoretical
models for herbivores (Kohn, 1996; Table 3) are grossly accurate, predicting LGM herbivore tooth enamel δ18O values of c. 17‰ vs. 17–
18‰ for average herbivore compositions there (Fig. 3). Using either empirical calibrations or inverting theoretical models, water compositions
at LBEC are estimated to have been ~−12‰ during the post-LGM Pleistocene. We do not know which specimens from LBEC are Holocene, so
we cannot independently estimate water δ18O values at that time.
During the LGM, all δ 13C values fall below the cutoff for C3 consumption (Fig. 7), so in principle no CAM, C4, or isotopically unusual
C3 plants (e.g. conifers) are required to explain compositions. High
δ 13C values do imply relatively arid conditions, which we discuss further in Section 5.5. Browsers (Odocoileus, Bootherium, and possibly
Antilocapra), exhibit lower δ 13C values than grazers and mixed
feeders (Bison, Camelops, Mammuthus and possibly Ovis; p b 0.001),
as expected because more open habitats tend towards 13C-enrichment (e.g. see Koch et al., 1998; Kohn et al., 2005). Although low
pCO2 during the LGM could stabilize or maintain C4 biomass relative
to C3 (Collatz et al., 1998; Koch et al., 2004), lower temperatures offset the C4 advantage (e.g. Ward et al., 2008). Also, C4 grass growth
depends on availability of summer moisture. All general circulation
models for the LGM predict lower temperatures at NTC, and many
predict drier summers (e.g., Hoffmann et al., 2000; Shin et al., 2003;
Braconnot et al., 2007), essentially destabilizing C4 grasses at that
time; implications for GCM accuracies and C4 biomass predictions
are discussed further in Section 5.6.
TR
Non-bison trajectory
Sangamon
Interglacial
LGM
post-LGM
Holocene
δ18O (‰, V-SMOW)
δ18O (‰, V-SMOW)
220.
Bootherium 45216
Bos 97862
Cervid 31504
Antilocapra 44853
Miracinonyx 43296
(+ 2‰)
Equus
Bison, Bso
Ovis
Canis lupus
Antilocapra
22.0
HM
18.0
nt
epende
Water-d trajectory
e
herbivor
Sangamon
Interglacial
Bos
?
-15.0
125
14.0
100 30
25
20
15
10
5
0
Age (ka)
Fig. 7. δ13C vs. time for Natural Trap Cave. δ13C values of hypergrazer (Bison) increases
in warmer climates, probably reflecting increase in percentage of C4 grass in local ecosystem. Equus show an analogous decrease from 110 ka to LGM. Browser (Antilocapra),
mixed feeder (Ovis), and carnivore (C. lupus) show no significant change. Error bars
represent 2σ age uncertainties, and 2σ variation in compositions. Dashed line shows
upper limit of δ13C values for C3 plants (Kohn, 2010), as adjusted for the δ13C value
of atmospheric CO2 (Smith et al., 1999).
LGM
10.0
125
100 30
25
post-LGM
20
15
Holocene
10
5
0
Age (ka)
Fig. 8. δ18O vs. time for Natural Trap Cave. δ18O values for water-dependent herbivores
increase from Last Glacial Maximum to Holocene (see also Kohn and McKay, 2010);
other herbivore compositions are consistent with this trend, but carnivore data are
not. The δ18O value from Sangamonian Equus is anomalously low.
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
During the latest Pleistocene, Bison and Ovis δ 13C values exceed
the C3 cutoff (slightly), as does Bison during the Holocene, and
Equus during the Sangamonian. In fact, δ 13C values for Bison increase
systematically by 2 to 7‰ from the LGM to the Holocene. Considering
that Bison is a hypergrazer, this increase likely reflects an increasing
proportion of C4 grass in diets and the overall environment. That is,
C4 abundances could well have been 0% during the LGM, and increased in the Holocene. Insofar as we can determine, this is the
first documentation of increasing C4 abundances across the Pleistocene–Holocene transition from carbon isotopes in tooth enamel
from North America. The compositions of all herbivores except Bison
and Equus, however, are consistent with an exclusively C3 diet, especially when considering seasonal shifts and isotope biases discussed
in Section 5.4.
5.2. Carnivore isotope compositions: evaluation of isotopic models
Theoretical models for carnivores (Kohn, 1996; Table 3) predict
similar or slightly lower δ 18O values relative to prey. Thus, carnivore
values of ~22‰ at NTC, and oxygen isotopic differences between carnivores and herbivores (Δ 18Ocarn–herb) of 4 to 5‰ are much greater
than anticipated. Some parameters in the carnivore models are either
adjustable for a specific physiology, such as daily water intake and
urine output, or constrained by few data, such as the oxygen isotope
fractionation between protein and water. Consequently we explore
the range of carnivore compositions that such models can explain,
and their implications for carnivore diet and physiology.
Most intake oxygen is derived from liquid water, both in food and
as drinking water (Luz and Kolodny, 1985). Large herbivore tooth
compositions imply body water compositions of c. − 8‰ (slightly
higher than predicted local leaf water compositions), and drinking
water compositions of − 15 to − 16‰ (Kohn and McKay, 2010).
Major changes to carnivore drinking water intake (low WEI model),
food δ 18O values (high δ 18O H2O and protein models), and high
vapor output all increase Δ 18Ocarn–herb by only 0.3 to 1.4‰ (Table 3).
Thus, error in a single variable cannot explain the model-data discrepancy. Taking extremes in all parameters (maximum carnivore
model) yields Δ 18Ocarn–herb ~ 2.5‰. While this result is still below observed values, it does illustrate that average carnivores may have
physiologies and diets far different than assumed by Kohn (1996).
Most importantly, carnivores in Wyoming may minimize liquid
water output and consume prey items much more 18O enriched
than currently modeled. Clearly, more research on carnivore oxygen
isotope compositions, possibly in controlled experiments, is needed.
The magnitude of Δ 13Ccarn–herb is slightly larger than anticipated.
Most work on bone suggests a value of −1 to − 1.5‰ (Clementz et
al., 2009), whereas we observe tooth enamel differences of −2 to
−2.5‰ at NTC. Previous studies might have underestimated
Δ 13Ccarn–herb, but several other explanations are possible including:
(1) Large herbivores may not be representative of carnivore diets
(Clementz et al., 2009), and instead more common prey may have
had lower δ 13C values. This view receives some support from the isotopic difference between small and large carnivores at LBEC, although
large canids and felids typically prey on large herbivores. (2) Carnivores preferentially consume fat-rich portions of prey, and fats
have lower δ 13C values than other components (e.g., DeNiro and
Epstein, 1977, 1978; Hilderbrand et al., 1996). (3) Carnivore teeth
mineralize rapidly post-weaning, so may be seasonally biased towards summer and autumn compositions when herbivore δ 13C
values are lowest. Again, experimental studies of carnivores may
help address these discrepancies between expected and observed
isotopic fractionations.
The δ 13C values of C. lupus appear to remain invariant through
time, but we have no modern or Sangamonian data from the region
with which to compare glacial and interglacial compositions. Arguably, the higher δ 13C values of C. lupus and Felis at LBEC could indicate
49
an increase in C4 biomass into the Holocene, but the absence of direct
dating of carnivores precludes definitive interpretation.
5.3. Extreme isotopic compositions
Whereas generalized models can explain many compositions, we
offer two main explanations for the extreme compositions observed
for several taxa — omnivory and climate-induced changes to diet.
First, ursids and small canids are omnivorous, so the diets and compositions of Vulpes, C. latrans, Ursus and Arctodus may have experienced
greater seasonal change than in other animals. If so, each tooth might
reflect only one small window within the total isotopic range sampled by these opportunistic animals. Thus, the >7‰ carbon isotope
difference in the single Ursus tooth at NTC vs. LBEC, and the nearly
5‰ difference between Ursus and Arctodus compositions at NTC
might simply reflect the range of δ 13C values that these animals sampled seasonally. This view is supported by minimal isotopic zoning
(b1‰) recorded in many teeth. Alternatively, different isotopic values
might reflect individual selectivity, so that some animals systematically record different compositions than other individuals of the
same species, even in the same area and time. This view is supported
by the NTC Ursus tooth, which exhibits nearly 4‰ isotopic variation in
δ 18O values, but only 0.5‰ variation in δ 13C values.
A second explanation for isotopic extremes notes that many of
these compositions at NTC occur for Holocene specimens. Possibly
Pleistocene–Holocene climate change caused divergence in isotope
compositions of different taxa, either because the environment diversified isotopically, so the same diet had a different composition, or individual taxa preferentially shifted their diets to isotopically extreme
foods. For example, Odocoileus carbon isotope compositions in the
southeastern US shifted downwards from the Pleistocene to Holocene, probably reflecting Holocene development of denser forests
(Koch et al., 1998; Kohn et al., 2005). These possibilities might be distinguished with a larger modern dataset that includes a range of herbivores and carnivores similar to those we analyzed from late
Pleistocene NTC.
We also note that few isotopic data exist for some ecosystem components, such as arthropods, which are consumed by omnivores. It
appears that the oxygen isotope composition of insect chitin and cellulose are broadly similar (Motz, 2000), but the fractionation between
water and chitin is only ~20‰ (Wang et al., 2009; Nielson and Bowen,
2010), whereas the water-cellulose fractionation is ~ 27‰ (Sternberg,
1989). Thus insect body water may have a much higher δ 18O value
than other water sources, including plants. Data from one study suggest that bumblebees are ~10‰ enriched in 18O over local water in
southern England (Wolf et al., 1996; Darling and Talbot, 2003;
Darling et al., 2003), whereas leaf water in the same environment is
probably only 5–7‰ enriched (e.g. Table 3). An experimental study
of vapor uptake in cockroaches (Ellwood et al., 2011) indicates they
can be over 10‰ enriched in 18O relative to water in dry environments. Although requiring further study, possibly insectivory leads
to 18O enriched compositions, and can help explain unusually high
δ 18O values for Vulpes and C. latrans, either directly or by consumption of insectivorous rodents.
5.4. Intratooth zoning
The 2–3‰ range in δ 18O values along the length of herbivore teeth
(Fig. 5) likely reflects seasonal changes to local water and plant compositions, with high and low values in the summer and winter respectively (Bryant et al., 1996; Fricke and O'Neil, 1996; Kohn, 1996; Kohn
et al., 1998). The isotopic seasonality of modern precipitation in the
western United States is commonly ~ 10‰ (Henderson and Shuman,
2009), so the measured range in teeth requires some degree of damping, either within soils, streams or lakes in the environment (Coplen
and Kendall, 2000; Henderson and Shuman, 2009), within the animal
50
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
(Kohn et al., 2002), or during the formation and maturation of tooth
enamel (Passey and Cerling, 2002).
Carbon isotope variations in herbivore teeth are considerably
smaller, with a common range b1‰ (Figs. 5–6). Because the δ 18O
maxima and minima recorded in teeth suggest that both summer
and winter compositions are recorded, the small variation in δ 13C
values suggests that large herbivores did not substantially vary their
diets seasonally, possibly in contrast to omnivores. Some published
data also illustrate seasonal inverse correlations between 18O and
13
C in large mammals (e.g., Bocherens et al., 2001; Wang et al.,
2008; Feranec et al., 2009; Biasatti et al., 2010, 2012; Zin-MaungMaung-Thein et al., 2011). Inverse correlations might result from a
combination of factors related to the seasonality of plant growth
and availability of different foods. Possible explanations for inverse
18
O– 13C correlations include the following:
(1) Monsoonal circulation. The standard interpretation of inverse
18
O– 13C correlations in southeast Asia is that intense, 18O-depleted, summer monsoonal precipitation stabilizes 13Cenriched C4 grasses (Wang et al., 2008; Biasatti et al., 2010,
2012). Although this process explains Asian data well, there
is no evidence for C4 grasses in Wyoming during the LGM,
when similar negative correlations also occur in our data, and
summer precipitation in Wyoming is 18O-enriched, not depleted.
This explanation does not seem viable for our study area.
(2) Moisture. Plant δ 13C values decrease with increasing moisture
availability (Farquhar et al., 1989; Kohn, 2010). If the summer
growing season were relatively wet, then high δ 18O summer
precipitation values would correspond with low δ 13C plant
values relative to other seasons.
(3) Seasonal dietary selection of same plants. New plant growth
does not generally occur during the winter, so herbivores
must rely on other food sources. Different tissues of the same
plant have different compositions, and leaf litter, bark, and
twigs are enriched in 13C relative to fresh leaves (Dawson et
al., 2002). Reliance on different tissues of the same plant during
the winter could increase δ13C values of herbivores.
(4) Seasonal dietary shift to conifers. Conifers have δ 13C values ~ 2‰
higher than deciduous angiosperms (Diefendorf et al., 2010),
so a winter dietary switch to conifers could increase herbivore
δ 13C values.
(5) Winter fat burning. Herbivores commonly accumulate fat reserves in the summer and autumn to guard against scarce winter food supplies. Lipids are 2–4‰ depleted in 13C relative to
coexisting proteinaceous tissues (e.g., DeNiro and Epstein,
1978; Hilderbrand et al., 1996). Because proteins are ≥5‰
enriched relative to total diet (e.g. Ambrose and DeNiro,
1986; Passey et al., 2005; Clementz et al., 2009), however, herbivore lipid reserves should be at least 2‰ enriched relative to
summer and autumn plant sources. Thus, preferential use of fat
reserves in the winter could increase δ 13C values.
There are too few data from carnivores to draw firm conclusions
regarding seasonal isotopic variations. An inverse correlation between δ 18O and δ 13C values, as suggested by one Miracinonyx tooth,
could simply indicate that carnivore compositions track herbivores.
That is, as herbivore δ 13C values increase in the winter and decrease
in the summer, so too do carnivore values. Alternatively and analogously to herbivores, if lipid δ 13C values in carnivores are higher
than in original prey, then winter use of fat reserves could cause an
increase in δ 13C and an inverse δ 18O–δ 13C correlation.
5.5. Critical evaluation of GCM's, 1. MAP and precipitation δ 18O
If we can identify exclusive C3 consumers, then their isotope compositions can be used to estimate MAP (Kohn, 2010). In the case of
NTC, we can consider either LGM compositions only, when no taxon
exceeds the C3 cutoff, or taxa other than Bison, Sangamonian
Equus, and possibly Ovis. Either approach yields average δ 13C values
of ~−10.0 ± 0.5‰, which is equivalent to modern C3 plant values of ~
−25.5‰ after accounting for isotopic fractionations and Pleistocene vs
modern δ13Catm. At an elevation of 1500 m and latitude of 45°N, this
value implies MAP ~ 150 ± 200 mm/yr (Fig. 2); approximately threequarters of the error results from the MAP calibration, which in turn reflects scatter in modern data. The remainder of the error corresponds to
the assumed uncertainty in mean δ13C of ±0.5‰. Average MAP today
near NTC is ~200 mm/yr (Kohn and McKay, 2010), so within uncertainty we can resolve no change to MAP between the late Pleistocene and
today. Even considering uncertainties, our data are consistent with a
relatively dry late Pleistocene, with MAP ≤ 350 mm/yr. This result is
consistent with models of vegetation structure over North America
during the LGM (e.g., Cowling, 1999), which suggest much more
open habitats at NTC and LBEC than occurring today.
Oxygen isotope compositions for the more water-dependent taxa
(Bison/Bos and Equus, Fig. 8) systematically increase from the LGM to
the present. The same trend is observed for Bootherium and Mammuthus (Kohn and McKay, 2010), and possibly also less waterdependent Ovis and Antilocapra (Fig. 8). As discussed previously
(Kohn and McKay, 2010), this trend is interpreted to reflect changes
to atmospheric circulation and the δ 18O value of local precipitation.
In general, precipitation that is 18O-depleted vs. -enriched derives
from the Pacific during the winter vs. the Gulf of Mexico during the
summer. Lower δ 18O values during the LGM are consistent with
GCM's that predict a decrease in summer precipitation and in annual
precipitation δ 18O overall (e.g., Hoffmann et al., 2000; Shin et al.,
2003; Braconnot et al., 2007). A decrease in summer precipitation,
however, would argue against wetter summers as the cause of inverse seasonal correlations between δ 18O and δ 13C in zoned teeth
(see above). Sangamonian Equus compositions are surprisingly low,
however, even below LGM values. Possibly, the single Equus specimen
has non-representative δ 18O values, although its δ 13C value is consistent with systematic carbon isotopic trends. Alternatively, Sangamonian atmospheric circulation may have been different from
Holocene circulation, with a greater proportion of Pacific moisture.
5.6. Critical evaluation of GCM's, 2. Shifts to C4 plant abundance
Following Connin et al. (1998) and Koch et al. (2004), we further
explore using modern correlations of C4 abundance with climate variables (Paruelo and Lauenroth, 1996) to evaluate the consistency of
GCM's with observed increases and decreases in C4 biomass. Climate
variables required for predictions include mean annual temperature
(MAT) and precipitation (MAP) as well as the ratio of June–July–August
(summer) precipitation to MAP (JJA/MAP). Unlike previous studies, we
quantitatively consider theoretical models of C3 vs. C4 competition
(Collatz et al., 1998) to correct for changes in pCO2. Essentially, we assume that the decrease in C3–C4 cross-over temperature associated
with decreased pCO2 offsets the GCM-predicted decrease in mean annual
temperature:
X C4 ¼ −0:9837 þ 0:000594ðMAP; mmÞ þ 1:3528ðJJA=MAP Þ
þ 0:2710 lnðMAT−ΔT X Þ:
ð3Þ
where XC4 is the fraction C4 biomass and ΔTX is the change in cross-over
temperature associated with a change to pCO2 (TX is negative for decreased pCO2). XC4 is calculated both for modern conditions and the
LGM; because absolute C4 biomass is difficult to evaluate from proxy
data, changes to XC4 are evaluated qualitatively.
Using NTC as an example, modern conditions of MAT=7.1 °C,
MAP=211 mm/yr, and JJA/MAP=0.31 predict 9% C4 biomass, consistent
with regional trends (Paruelo and Lauenroth, 1996). The PMIP2 ensemble
averages predict lower MAP (c. 100 mm/yr), no change to JJA/MAP, and a
12–13 °C decrease in MAT. However, relative to a modern reference pCO2
M.J. Kohn, M.P. McKay / Palaeogeography, Palaeoclimatology, Palaeoecology 326–328 (2012) 42–53
of 350 ppmV (Collatz et al., 1998), the LGM pCO2 of 185 ppmV used in
PMIP2 (Braconnot et al., 2007) decreases the C3–C4 crossover temperature by 11–12 °C; thus we calculate LGM C4 biomass using Eq. (3) at
MAT−TX =7.1–12.5−(−11.5)=6.1 °C, MAP=100 mm/yr, and JJA/
MAP=0.31. This yields a calculated value of −2%, i.e. zero, consistent
with our carbon isotope data. The calculated %C4 is rather sensitive
to JJA/MAP and MAT, and increasing JJA/MAP to 0.39 or MAT by
1 °C yields the same predicted %C4 as modern conditions. That is,
the observation of lower LGM C4 abundances at NTC provides a sensitive check on GCM accuracy, and closely validates the PMIP2 ensemble average.
Similar calculations using PMIP2 for some other localities in the US
are also broadly consistent with C4 plant distributions. Predictions for
Texas imply similar or slightly greater %C4 during the LGM, consistent
with tooth enamel isotope data that indicate significant C4 biomass
(Koch et al., 2004). This result supports Koch et al.'s conclusion that
decreased pCO2 helped stabilize C4 ecosystems in some regions during
the LGM despite decreased temperature. Applications to Florida are
especially interesting because C4 plant biomass increased in central
Florida during the LGM (Huang et al., 2006) yet also exhibited a geographical, northward-decreasing gradient in abundance (Feranec,
2004b). An increase in precipitation in southern Florida during the
LGM and relatively small temperature decrease is predicted to have
increased C4 biomass, whereas a decrease in JJA/MAP in northern
Florida offset the effect of pCO2, implying no change to C4 abundance
there. Central Florida is predicted to exhibit an increase in C4 biomass. Thus, again combination of PMIP2 with Eq. (3) broadly predicts
observations. Although we recognize complexities in predicting C4
biomass abundance, especially the use of empirical correlations
from the western US alone and absence of a first principles model
for plant competition, the dependence of C4 biomass on pCO2, temperature, and growing season precipitation recommends its use in validating climate models (Connin et al., 1998).
6. Conclusions
(1) Pleistocene diets and ecosystems were dominated by C3
plants, but Bison documents increasing C4 from the Pleistocene
to Holocene. A single Sangamon Equus tooth also has elevated
δ 13C, suggesting that C4 abundances generally increase in central and eastern Wyoming during interglacial periods.
(2) Compared to herbivores, carnivores exhibit unexpectedly high
δ 18O and low δ 13C values, indicating a poor understanding of
carnivore diets and physiologies. Likely sources of error include
knowledge of liquid water outputs and isotopic compositions
of prey.
(3) Herbivore intratooth zoning commonly shows negative correlations between δ 18O and δ 13C. Possible explanations include
relatively wet summers, seasonal changes in diet emphasizing
drier plant tissues or conifers during winter, and winter burning of fat reserves.
(4) Oxygen isotope values increased systematically from the Pleistocene to Holocene (Kohn and McKay, 2010), consistent with
general circulation models that show an increased proportion
of Pacific moisture during the LGM (Hoffmann et al., 2000;
Shin et al., 2003; Braconnot et al., 2007).
(5) Mean annual precipitation is estimated from LGM δ 13C values
at ≤350 mm/yr, similar to modern conditions (c. 200 mm/yr).
(6) Changes to C4 biomass abundance can provide a sensitive test
of GCM accuracy; PMIP2 simulations in combination with a
modified equation for C4 plant abundance explains observations at NTC (this study), central Texas (Koch et al., 2004),
and Florida (Koch et al., 1998; Huang et al., 2006), including
C4 abundance decreases in some areas and increases in others.
51
Acknowledgments
We are extremely grateful to Drs. Larry Martin and Tonia S. Culver
at the Natural History Museum and Biodiversity Research Center, University of Kansas, and at the University of Colorado Museum of Natural History, for making so many specimens available for isotopic
analysis, and Daniel Williams for his help deciphering 14C ages and
NTC stratigraphy. We thank R. Feranec and two anonymous reviewers
for providing detailed reviews that substantially improved the paper,
and J.M. Law for laboratory assistance. Funded by NSF grants ATM
0400532 and EAR 0819837 to MJK.
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