Download Dietary niche partitioning among fossil bovids in late Miocene C3

Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529 – 538
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Dietary niche partitioning among fossil bovids in late Miocene C3
habitats: Consilience of functional morphology
and stable isotope analysis
Faysal Bibi ⁎
Department of Geology & Geophysics, Yale University, PO Box 208109, New Haven, CT 06520-8109, USA
Received 11 May 2007; received in revised form 22 June 2007; accepted 26 June 2007
Abstract
Teeth of late Miocene bovids referred to Bovini and “Boselaphini” were subjected to enamel stable carbon and oxygen isotope analysis to
test paleoecological reconstructions based on dental morphology. Teeth of Bovini possess derived characters–including larger size, higher
crowns, and increased enamel surface area–that are indicative of feeding on a more fibrous and gritty diet, probably grass. In contrast, teeth
of “Boselaphini” reflect the plesiomorphic condition among bovids–being smaller, lower-crowned, and with simple occlusal morphology–
and are indicative of a diet with a greater reliance on softer food items such as browse. Late Miocene bovines are also expected to have
inhabited drier, more open habitats than did boselaphines. Stable carbon and oxygen isotopic compositions from 30 fossil teeth (18 bovine,
12 boselaphine) from well-dated localities of between 8.3 and 7.9 Ma in age from the Siwalik deposits, Pakistan, were analyzed to test these
paleoecological hypotheses. All δ13C values (VPDB) are more negative than −8‰, indicating that both bovines and boselaphines at this
time had pure C3 diets. The mean δ13C for bovine teeth (−10.4‰) is more positive than that for boselaphines (−10.9‰), and the differences
between these two series are significant (Wilcoxon, pb 0.01; t test, p b 0.05) while the variances are not. Early bovines thus appear to have
exploited more open habitats than did their boselaphine counterparts. Lack of a significant difference between variances suggests that the
dietary niche breadth of early bovines was not different from that of boselaphines. Mean δ18O (SMOW) for bovine teeth (26.3‰) is slightly
more negative–as might be expected for grazers–but not statistically significant from the boselaphine δ18O mean (28.1‰, t test, p= 0.066).
Overlap in δ18O values between bovines and boselaphines is high, implying that these two bovid types did not differ greatly in their water
intake behaviors. Rather, both fossil bovines and boselaphines probably shared similar obligate drinking habits and dependency on water
bodies much as living boselaphines, bovines, and tragelaphines (clade Bovinae) do today.
Stable isotope analysis results, particularly δ13C values, suggest that in the late Miocene neither bovines nor boselaphines
inhabited dense forest habitats. And while both bovid taxa may have been mixed feeders to different extents, the δ13C values
support the hypothesis developed on the basis of dental functional morphology that early bovines evolved inhabiting more open
habitats than did contemporaneous boselaphines. The scenario whereby the bovine clade owes its origins to a boselaphine lineage
that adapted to drier, more open habitats is supported by the general context of climatic and faunal change in Eurasia in the late
Miocene, particularly between 11–8 Ma, when faunal assemblages from many sites exhibit significant turnover events through
which open-habitat taxa become present in increasing proportions at the expense of closed-habitat taxa.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Bovidae; Bovinae; Bovini; Boselaphini; Late Miocene; Siwaliks; Grasslands; Diet; Paleoecology
⁎ Fax: +1 203 432 3134.
E-mail address: [email protected].
0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2007.06.014
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F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
1. Introduction
The earliest representatives of the bovid clade Bovini
were recently identified from late Miocene fossil
collections from the Indian Subcontinent (Bibi, 2007).
The extant crown clade Bovini comprises grazing
species such as buffaloes, bison, and cattle. The earliest
bovines can be identified by dental remains from the
Siwalik deposits, Pakistan, dated at least as far back as
8.9 Ma. These dental remains are distinguished from
those of ancestral and contemporaneous boselaphine
bovids primarily by their significantly larger size, higher
crowns, larger basal pillars, and more complicated
enamel outlines (Fig. 1). Taken together, these adaptations reflect an increased intake of rougher, more fibrous
or gritty foods in early bovines, such as grasses, leading
to the supposition that early bovines evolved exploiting
more open habitats than did ancestral and contemporaneous late Miocene boselaphine bovids that lacked these
dentognathic adaptations (Bibi, 2007). These inferences
based on functional morphology are tested here using
stable isotope compositions of tooth enamel to examine
the feeding characteristics of late Miocene bovines and
boselaphines.
At tropical latitudes today most grasses utilize the C4
photosynthetic pathway that promotes survival in seasonally arid or heat-stressed regions (Tipple and Pagani,
2007). However, stable carbon isotopic evidence suggests
C4 grasses did not substantially expand in the Siwalik
region until after 8.1 Ma, with C4-dominated habitats first
appearing by 7.4 Ma (Barry et al., 2002; Quade and
Cerling, 1995; Quade et al., 1989). This suggests that if
the earliest bovines evolved by exploiting more open
habitats, the terrestrial environment must have been
dominated by C3 floras, potentially C3 grasslands. Stable
Fig. 1. Examples of late Miocene bovine and boselaphine teeth
analyzed in this study. Bovine teeth (left, YPM 19681) are larger, with
developed basal pillars, more convoluted enamel ridges, and higher
crowns than contemporaneous boselaphine teeth (right, YPM 19613).
Both teeth shown are right upper second molars in mid wear stages.
Scale bar equals 1 cm.
carbon isotope analysis distinguishes readily between C3
and C4 plants, with C3 plants displaying bulk organic
carbon δ13C values between −35‰ and −22‰ and C4
plants between −19‰ and −9‰ (Bender, 1971; Cerling
and Harris, 1999). Plant δ13C is an inverse function of the
ratio of the partial pressure of CO2 in leaf intercellular
spaces (ci) relative to that in the atmosphere (ca) (Farquhar
et al., 1982a; Farquhar et al., 1982b) and as a result even
within either of the C3 or C4 ranges there is an observed
correlation with increasingly enriched δ13Cplant values
and increasingly heat- or water-stressed environments
(Ehleringer and Cooper, 1988; Farquhar et al., 1989). For
example, Medina and Minchin (1980) and van der Merwe
and Medina (1991) found that leaves growing in subcanopy conditions had more depleted δ13C values than
those growing at canopy level and in clearings. This
phenomenon is ascribed to two factors: (1) the ‘canopy
effect’ whereby δ13C-depleted CO2, released as a result of
decomposition of leaf litter at ground level, is photosynthetically recycled by plants growing nearer to the forest
floor (Vogel, 1978); and (2) the observed relationship
between plant water-use efficiency and δ13C, whereby
unstressed plants growing in shaded/humid/low-salinity
conditions will maximize the kinetic (at the stomatal
level) and physiological (at the level of the enzyme
rubisco) fractionation that discriminates against fixation
of the heavier isotope of carbon, 13C (Farquhar et al.,
1982a; O'Leary, 1993; van der Merwe and Medina,
1991). Conversely, increases in stressors such as light
intensity, salinity, and aridity require plants to combat
excessive evaporation by closing leaf stomata (i.e. decreasing stomatal conductance) for longer periods of time,
trapping a limited reserve of CO2 in the leaf and resulting
in fixation of a greater proportions of the heavier isotope
of carbon than would occur under more optimal
conditions (Farquhar et al., 1982a; van der Merwe and
Medina, 1991). Studies have shown that decreased shade
or water availability can effect δ13C changes of about +1–
2‰ in any single plant species (Ehleringer and Cooper,
1988; Michelsen et al., 1996). Changes in the partial
pressure as well as the 13C/12C ratio of atmospheric CO2
can also affect the resulting δ13C value of plant material
(and hence herbivore tooth enamel). Given that both the
partial pressure and 13C/12C ratio of pre-industrial
atmospheric CO2 do not appear to have changed
significantly since the late Miocene (Pagani et al., 1999;
Pagani et al., 2005; Passey et al., 2002), δ13C values of
fossil teeth examined in this study are interpretable in
reference to δ13C endmember values in modern systems.
The δ13C values of plants translate directly to the δ13C
values in tissues of the mammalian herbivores that feed on
them. Large ruminant enamel bioapatite is enriched in 13C
F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
by about +14.1 ± 0.5‰ with respect to the plant source
(Cerling and Harris, 1999), with living bovines averaging
slightly greater values of approximately +14.6 ± 0.3‰
(Cerling and Harris, 1999; Passey et al., 2005). Bovids
feeding on pure C3 diets should exhibit ranges between
about −21‰ and −8‰, with open-habitat species having
more positive values than forest/canopy species. This is
confirmed by studies of living ungulates, such as a study
of African bovids (Cerling et al., 2003) which determined
that duiker species (Cephalophus spp.), which inhabit
rainforests and forests, exhibit much more negative δ13C
values than the eland (Tragelaphus oryx), a woodlandsavanna species, though both of these bovids are
exclusive C3 feeders. Similarly, contrasts between closed
and open-habitat bovids in the ancient record can be tested
by evaluating tooth enamel δ13C values of specific species. Within a defined age and region, fossil bovids that
inhabited more open habitats should exhibit more positive
δ13C values than those that inhabited more closed habitats. Analogous studies comparing δ13C values within the
C3 range among various fossil ungulates have been performed with relative success on Miocene herbivore communities from Panama (MacFadden and Higgins, 2004),
Turkey (Quade et al., 1995), and Florida and California
(Feranec and MacFadden, 2006).
The oxygen isotope composition of bovid tooth
enamel was analyzed in order to test for differing patterns of water intake between bovine and boselaphine
fossil bovids. Due to evaporative enrichment, leaf water
δ18O values are typically10–30‰ more positive than
the meteoric source (Yakir, 1997). As a result, mammal
species that obtain the majority of their water from the
plants they eat should exhibit more positive δ18O values
than those that are obligate drinkers (e.g. Sponheimer
and Lee-Thorp, 1999; Sponheimer and Lee-Thorp,
2001). Sponheimer and Lee-Thorp (1999) found that
browsers tend to have slightly more enriched δ18O
values than do grazers. On this basis, Miocene fossil
boselaphines should be slightly more enriched in 18O
than fossil bovines. This expectation is not strong,
however, given the water-use habits of the living
relatives of these fossils. Living bovines are obligate
drinkers with strong affinities to water, exemplified by
the water buffalo (Bubalus bubalis), which spends much
time fully immersed in water. Among bovine outgroups,
the chousinga (Tetracerus quadricornis, a boselaphine)
and most tragelaphines (Tragelaphus spp.) are water
dependent as well (Estes, 1991; Prater, 1965). Given the
behavior of these extant species, water intake behaviors
of ancient boselaphines and bovines likely depended
more on varying local conditions such as water sources
(e.g. seasonal waterholes vs. rivers vs. perennial lakes)
531
and climatic variables (e.g. changes in annual precipitation patterns) rather than clade-specific ecological
attributes.
This study utilizes stable isotope analysis to test
hypotheses and predictions made on the basis of
functional morphological differences between teeth of
late Miocene bovines and boselaphines from the Siwalik
deposits. Primarily, stable isotopes are used to test
whether dietary intake differed in any significant way
between these two bovid groups. Bovines are expected
to display more positive δ13C values, indicating that
they fed in more open C3 habitats than did boselaphines,
and more depleted δ18O values as noted for grazing
herbivores that have a greater reliance on meteoric
sources for their water needs. Results of the analysis are
discussed with implications for the early evolution of
Bovini within the context of late Miocene climatic and
paleoenvironmental changes.
2. Methods
Thirty fossil specimens were selected for analysis
based on their morphology and stratigraphic provenance
(Table 1). Eighteen specimens are of early bovines (teeth
traditionally referred to Selenoportax or Pachyportax),
while twelve are of large non-bovine boselaphine fossils
(likely Tragoportax) that in this paper will be referred to
simply as boselaphines. Sites chosen and their ages are as
follows: L008 (8.331 ± 0.04 Ma), L011 (7.926 ± 0.12 Ma),
L012 (7.926 ± 0.12 Ma), L056 (7.926 ± 0.12 Ma), L073
(8.018 ± 0.31 Ma), and L074 (8.018 ± 0.31 Ma) (age
determinations from Barry et al., 2002).
Enamel was sampled using a Foredom rotary drill at
low speeds, fitted with a 33.5-gauge (0.5 mm diameter)
inverted cone carbide burr. Between 2000 and 6000 μg of
enamel was removed along a single transect from the base
to the tip of the crown, typically along either of the buccal
ribs (metacone or paracone) on upper teeth or lingual ribs
(metaconid or entoconid) on lower teeth, making sure to
include no cementum or dentine in the sample. Enamel
powder was treated with hydrogen peroxide and acetic
acid to remove effects of contaminant organics and
inorganic carbonate (Koch et al., 1997). Enamel was
treated with 30% H2O2 for between 24 to 48 h, decanted
and washed with distilled de-ionized water, then reacted
with 0.1 N acetic acid for 4 h, after which samples were
decanted and washed. Ethanol was added and samples
were dried overnight. The treated enamel was dissolved in
100% phosphoric acid and the resulting CO2 was
analyzed with a Gas Bench II coupled to a Thermo
Finnigan DeltaPlus XP mass spectrometer at the Earth
Systems Center for Stable Isotopic Studies, Yale
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F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
Table 1
Sample identification information and δ13C and δ18O values
Sample number
FB-10
FB-02
FB-04
FB-08
FB-09
FB-21
FB-23
FB-24
FB-26
FB-12
FB-17
FB-14
FB-25
FB-11a
FB-01
FB-05a
FB-22
FB-13
FB-18
FB-19
FB-28
FB-32
FB-34a
FB-36
FB-15
FB-16
FB-27
FB-29
FB-30
FB-35a
YPM number
19591
20018/19994
19613
20001
20026
19615
19610
49799
20024
19989
19502
49758
19281
19601
20022
20016
20002
19980
19499
19507
19500
19506
19504
19505
19678
19681
19680
19677
19679
19674
Taxon
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
“Boselaphini”
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
Bovini
δ13C (PDB)
−10.98
−10.77
−11.62
−11.15
−10.74
−10.11
−11.18
−11.41
−9.81
−11.16
−10.71
−11.23
−11.79
−10.60
−12.21
−10.30
−10.71
−10.50
−9.72
−9.63
−10.25
−10.09
−10.02
−10.53
−9.83
−10.20
−9.70
−9.85
−10.20
−10.68
δ18O (SMOW)
32.64
28.79
25.43
28.26
27.75
27.09
27.72
26.39
28.04
32.16
22.70
29.91
26.44
29.10
22.36
24.00
29.77
31.13
25.31
24.94
25.76
25.99
27.58
24.73
27.26
23.86
24.89
28.64
26.53
25.69
Mass (μg)
4538
4346
4316
2197
2474
1897
1055
1140
2173
3209
2627
2361
4241
3359
3002
3348
1415
4735
4272
4312
3493
3301
2231
3696
3754
2474
4287
5542
4339
4595
Tooth sampled
X
M
M3
M3
M3
M3
M3
M3
M3
M3
M3
M3
MX
M3
M3
M1or2
M3
M1or2
M1or2
M3
M3?
M1
M1or2
M3
M3
M3
M2
M1or2
M1
M3
M3
Locality
L011
L012
L012
L012
L012
L012
L012
L012
L012
L056
L073
L074
L008
L011
L012
L012
L012
L056
L073
L073
L073
L073
L073
L073
L074
L074
L074
L074
L074
L074
YPM, Yale Peabody Museum. For tooth abbreviations, M denotes molar and superscripts and subscripts denote upper and lower teeth positions,
respectively, with x indicating indeterminate tooth position.
University. Standards run with the bovid enamel sample
included NBS-18, NBS-19, Lincoln Limestone, and the
MEme fossil proboscidean standard. For MEme, average
run values of −10.37 for δ13C and 25.75 for δ18O were
used (L. R. G. DeSantis pers. comm.). Carbon and oxygen
isotope values are reported relative to isotopic standards
such that
d13 C or d18 O ¼ ðRsample =Rstandard # 1Þ % 1000
where Rsample and Rstandard are the 13C/12C or 18O/16O
ratios of the sample and standard, respectively. δ13C values
are reported relative to the Vienna PeeDee Belemnite
(VPDB) standard, while δ18O values are against the
Standard Mean Ocean Water (SMOW) standard.
Shapiro–Wilk tests were performed on all sample
series values to determine whether distributions were
normal or not. For all samples, F tests and Student's t
test assuming equal variances were used. For nonnormal distributions, the non-parametric Wilcoxon two-
sample test (equivalent to Mann–Whitney U test) was
used in addition. Statistical tests were performed using
JMP 6.0 software. Significance was set to α = 0.05.
3. Results
3.1. Carbon isotope ratios
The total range of variation for all values is just under
3‰, ranging from −12.2‰ to −9.6‰ (Fig. 2, Table 1).
The mean δ13C value for all 18 bovine samples is
−10.4‰ (range −12.2‰ to −9.6‰) while for the 12
boselaphine samples the mean is −10.9‰ (range −11.6‰
to −9.8‰). Shapiro–Wilk tests reveal that while
boselaphine δ 13 C values are normally distributed
(p N 0.05), bovine δ13C values are not (p = 0.0058), and
so a Wilcoxon test was performed along with the t test. An
F test determined that variances between bovine and
boselaphine δ13C values were not significantly different.
Both the Wilcoxon and t test indicate that bovine and
F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
Fig. 2. Tooth enamel δ13C and δ18O values for all specimens analyzed
(A) and δ13C values for all specimens separated by locality (B).
boselaphine δ13C values are significantly different (twosample Wilcoxon, p b 0.01; t test, p = 0.0316). The δ13C
values of bovine and large boselaphine teeth separate at
−10.7‰ although two bovine samples display δ13C
values more negative than −10.7‰, these in fact being the
two most negative values recorded among all thirty
samples analyzed. Likewise, among the boselaphine
samples, two exhibit δ13C values more positive than
−10.7‰ though both these samples remain more negative
than the most enriched bovine samples (Fig. 2).
3.2. Oxygen isotope ratios
The δ18O values for all samples range between 32.6‰
and 22.4‰. Means for the 18 bovine and 12 boselaphine
samples are 26.3‰ and 28.1‰, respectively. Shapiro–
Wilk tests reveal that boselaphine and bovine δ18O values
are each normally distributed (p N 0.05), a two-sided F test
between bovine and boselaphine δ18O values indicate that
sample variances are not significantly different, and a twotailed t test finds that the difference between the means is
not significant (p = 0.066).
4. Discussion
4.1. Carbon isotope ratios—paleodiets
In general, ranges of carbon isotope values follow the
relationships predicted on the basis of functional mor-
533
phological differences between teeth recognized as early
Bovini and teeth attributable to other fossil boselaphines
(Bibi, 2007). However, in each series, outliers exist that
fall far from their respective series' means. Most of
the outlier values derive from locality 12 (Fig. 2B)
where there is no clear separation between bovines and
boselaphines along the δ13C axis. Locality 12 is the
single locality from which the greatest number of
samples came. This locality is quite rich in boselaphine
material, only a portion of which was sampled for this
study, but poor in bovine material (3 specimens only),
all of which was included in this study. The relative
abundance of boselaphines with respect to bovines may
indicate that locality 12 sampled paleohabitats that were
more favorable to the former at the expense of the latter.
However, it is not clear why this locality should produce
outliers in both series, that is, one bovine with very 13Cdepleted values and two boselaphines with relatively
13
C-enriched values (Fig. 2B). The one other outlier is a
very 13C-depleted bovine specimen from locality 8, a
locality from which no boselaphines were available for
comparative analysis. It is important to recognize that
though this work evaluates individuals that probably
derive from only two higher taxonomic groups (Bovini
and “Boselaphini”) it could potentially include three,
four, or more species. This is almost certainly the case
simply judging by the range in size (particularly among
the bovine specimens) and morphology (particularly
among the boselaphines) exhibited within the two
series. Species-level determinations are currently not
possible with any confidence on the isolated dental
material used here so this must remain an uncontrolled
variable in the current study. As a result, it is also
possible that samples with outlying carbon isotope
values represent particular species unrecognizable on
the basis of dental morphology alone. Further isotopic
sampling using more complete fossil material from other
collections may help resolve this issue. Despite the
coarse taxonomic resolution of this study, bovine and
boselaphine dental δ13C values are on average distinctive, with boselaphines exhibiting more 13C-depleted
values and bovines more 13C-positive values, with
statistically significant differences between these two
series. These findings attest to the strength of functional
morphology to draw paleoecological conclusions regardless of lower-level taxonomy.
Teeth of early bovines are characterized by the acquisition of several advanced characters that indicate an
increased ratio of tougher food items in the diet. These
characters include increased crown height, the enlargement of pillars (entostyles and ectostylids), the complication of enamel ridges, and greatly increased size (Bibi,
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F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
2007). Increases in crown height are an adaptation to
increased rates of wear, and it is known that the
consumption of grasses by herbivores produces greater
tooth wear than would occur with strict adherence to a
diet of leaves primarily because grasses are closer
to ground level and so naturally result in greater intake
of hard soil particles by the grazer (Mainland, 2003;
Sanson et al., 2007). In contrast, teeth of fossil
boselaphines, both ancestral to and contemporaneous
with Bovini, lack these advanced characters and remain
quite primitive in overall morphology. Among living
bovids, tragelaphines, species of which are primarily
browsers (Tragelaphus spp.), retain the primitive dental
morphological condition least changed from that of the
common ancestor of all the Bovinae (Bovini +Boselaphini + Tragelaphini).
Though early bovines appear to have evolved to
handle a diet composed of more abrasive foods, they did
so in the early late Miocene (by at least 8.9 Ma, Bibi,
2007), well before the expansion and dominance of
grasslands by heat-tolerant C4 grasses which took place
at 7.4 Ma in the Siwaliks sequence (Barry et al., 2002).
As such, it is most likely that early bovines evolved
feeding increasingly on C3 grasses and inhabiting more
open C3 grassland environments. The fact that all of the
samples analyzed here presented δ13C values more
negative than −8.0‰ establishes that bovine diets in the
Siwaliks at around 8 Ma were purely C3-dominated,
including no significant component of C4 plants.
Even within the C3 range, significant differences do
exist between δ13C values of bovine and boselaphine
fossil enamel, with bovine teeth having slightly higher
δ13C. Such enrichment is only to be expected if the
bovines were feeding on plants that themselves were
slightly enriched in 13C. It has been shown that C3 plant
δ13C values become progressively more positive with a
change from a sub-canopy mesic to open xeric environments, due to the canopy effect (Medina and Minchin,
1980; van der Merwe and Medina, 1991; Vogel, 1978)
and plant water-use efficiency responses to increased
heat stresses in open environments (Farquhar et al.,
1982a; O'Leary, 1993; van der Merwe and Medina,
1991). As a consequence, the differences in δ13C values
between bovine and boselaphine fossil bovids presented
in this study indicate that early bovines evolved exploiting more open environments than did boselaphines.
The fact that the means of these two series differ by less
than 1‰ suggests that the environmental/dietary differences between late Miocene bovines and boselaphines,
though distinctive, were not extreme. For example, in a
study of mammals from the Ituri Forest (Cerling et al.,
2004), sub-canopy dwellers including the dwarf ante-
lope (Neotragus batesi) exhibited an average δ13C value
of −22.8‰, more than 5‰ lighter than that of gapclearing inhabitants including sitatunga (Tragelaphus
spekei). In contrast, the less than 1‰ separation between
δ13C means of late Miocene bovine and boselaphine
teeth is comparable to the differences in mean values
recorded for species inhabiting similar environments
such as lesser kudu (Tragelaphus imberbis) and greater
kudu (Tragelaphus strepsiceros) from modern xeric
bushlands in Kenya (Cerling et al., 2003), both species
being C3 feeders in thicket or riverine forest habitats in
arid environments. The actual diets of the fossil bovines
and boselaphines and those of these living tragelaphines
are not comparable, however, as the fossil taxa may
have included significant quantities of C3 grasses in
their diets while living tragelaphines feeding on a substantial amount of grass would display δ13C values
more positive than −8‰ given that tropical grasses are
predominantly C4 plants.
It is likely that both the early bovines as well as the
fossil boselaphines sampled inhabited some form of
open C3 habitat, perhaps open forest or mosaic woodland-grassland environments where the boselaphines
would more selectively feed on browse and fresh grass
shoots while the early bovines would have an expanded
diet that overlapped with the boselaphines but included
also more of the tougher grasses. The reconstruction of
mixed diets for both these taxa but with relatively
greater dietary roughage in Bovini is in concordance
also with the results of tooth cusp mesowear analysis
(Bibi, 2007; Fortelius and Solounias, 2000). Dietary
separation between these two bovid groups may have
only been seasonal. Many studies (Bell, 1969; Dekker
et al., 1996; Schuette et al., 1998; Traill, 2004) have
shown that dietary behaviors among different sympatric
African bovids can be remarkably similar during the wet
season–when resources are not limiting–but can come
to differ greatly with the first onset of the dry season
when the food items that were every species' favored
food items become scarce or altogether depleted. Bell's
(1969) study of feeding behaviors among gazelle
(Gazella thomsoni), topi (Damaliscus korrigum), wildebeest (Connochaetes taurinus), zebra (Equus burchelli), and savanna buffalo (Syncerus caffer) found that
the larger species were able to include greater quantities
of the medium to tall grasses that are less nutritious but
more plentiful during the dry season than the more
protein-rich short grasses that all these herbivores
favored during the wet season. This is largely explained
by the fact that larger animals have relatively lower
metabolic requirements than smaller ones (Hungate
et al., 1959; Bell, 1969). The observation that herbivore
F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
body size is inversely correlated with the nutrient
content of their food (protein to fiber ratio) has been
dubbed the Jarman–Bell principle (Bell, 1971; Codron
et al., 2007; Geist, 1974; Jarman, 1974) and has been
used to relate body size, population structure and biomass, and habitat preferences in a variety of ungulates.
Using these same principles, one can reconstruct the
ecological context of late Miocene boselaphines and
bovines. With the evolution of added chewing surfaces,
increased crown height, and larger size (Fig. 1), early
bovines were adapting to pressures selecting for the
ability to incorporate more fibrous and less nutritious
food items in their diet.
4.2. Paleoclimate and evolution
The selective pressures that drove the evolution of
grazing morphologies were likely a consequence of
physical environmental changes that resulted in the
creation of more open habitats at the expense of more
closed ones. Numerous studies point to exactly this type
of mesic–xeric environmental change during the early
late Miocene, between about 11–8 Ma, in the Siwaliks
region but also in Eurasia as a whole (Damuth et al.,
2002; Fortelius et al., 2002; Fortelius et al., 2006;
Franzen and Storch, 1999; Quade and Cerling, 1995).
The late Miocene evolution of Bovini within the context
of ecological change is consistent within the general
picture of faunal turnover in the Siwaliks at the same
time. Isotopic evidence suggests shifts towards drier,
more seasonal environments at around 9.2 Ma, with C4
grasses beginning to establish by 8.1 Ma, and the first
C4-dominated habitats (paleosol carbonate δ13C values
greater than −4‰) appearing at 7.4 Ma (Barry et al.,
2002; Quade et al., 1989). Barry et al. (2002) note that
two of three major episodes of faunal turnover take
place around this time, in the period between 8 and
7 Ma. The nature of the faunal changes during this time
appear also to be consistent with the isotopic vegetational reconstructions, with increasing proportions of
open-habitat taxa at the expense of closed-habitat taxa
(Barry et al., 2002). The primary physical climatic
change that produced these environmental changes appears to have been increased seasonality (Quade et al.,
1989), with stronger precipitational contrasts between
wet and dry seasons occurring during this time. In
particular, the significance of seasonal intensification in
terms of a drier or prolonged dry season that could no
longer support the previously greater extent of forested
habitats should be emphasized. In concert with increasing aridity, new annual fire regimes may have
played an important role in the development of late
535
Miocene open habitats (Bond and Keeley, 2005; Keeley
and Rundel, 2005). The evolution of Bovini in the
Siwaliks region in the late Miocene then appears to have
been part of a greater wave of faunal change and adaptation in response to the development of drier, more
seasonal, open habitats.
Unlike early bovines, late Miocene boselaphines appear to have responded to these climatic and environmental changes with less ‘drastic’ measures, maintaining
what is essentially primitive dentognathic morphology.
These fossil boselaphines may have been ecologically
analogous to living tragelaphines (such as the greater and
lesser kudus mentioned above) that restrict themselves to
forested micro-habitats within generally more arid and
open environments, thus ensuring a perennial, though
spatially restricted, supply of browse-based foods such
as leaves, herbs, and fruits.
4.3. Morphological innovation and niche breadth
It has been suggested (Bibi, 2007) that the morphological novelties characterizing the earliest Bovini probably resulted in the ability of these bovids to expand
their dietary spectrum rather than to simply shift it over,
a phenomenon that has been observed in other grazeadapted fossil mammals (Feranec, 2003; Feranec, 2004;
Feranec, 2007). To use Hutchinson's (1957) terminology, early bovines, in evolving new morphologies,
might have expanded their fundamental niche, though
not necessarily their realized niche. The results of the
current study in fact provide no good evidence for either
a broadening or a narrowing of the fundamental niche:
while the fossil bovines do show a greater absolute
range of δ13C values than do the boselaphines (Fig. 2),
the variances themselves are not statistically significant,
implying that these groups maintained essentially similar dietary niche breadths (Feranec, 2007). Therefore,
the fundamental niche of early bovines appears simply
to have shifted over (indicated by more positive δ13C
values) relative to that of boselaphines, without evidence for any broadening. However, the fact that the
entirety of the measured values lie ‘crowded’ at the most
positive end of the possible C3 range may confound the
ability to perceive broadened niches using δ 13 C
analysis. There is also the possibility that early bovines
retained the ability to feed in more closed habitats but
only did so rarely, erratically, and when forced to. With
regard to living bovines, this may be illustrated in the
example of the African savanna buffalo (Syncerus
caffer), which throughout the year prefers grazing in
grasslands but will move to forest browsing if their
preferred riverine grassland habitats are occupied by
536
F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
wildebeest (Connochaetes taurinus) during the dry
season when resources are limiting (Sinclair, 1977).
Further work, such as serial sampling for determination
of within-specimen isotopic variability (amplitude of
seasonal signals), may better address this hypothesis
(e.g. Cerling et al., 2006; Nelson, 2005). Such work
would include preferably specimens identified to the
level of species and from a wider chronological range
extending into times when C4 became a prominent
dietary component.
4.4. Oxygen isotope ratios—water intake behaviors
Oxygen isotope ratios in the fossil bovine and
boselaphine teeth display means that are different but
not significantly so. Sponheimer and Lee-Thorp (1999)
found that browsers tend to exhibit slightly more enriched δ18O values than grazers, the interpretation being
that browsers derive a greater ratio of their water directly
from their food than do grazers. The fact that the fossil
boselaphine teeth are on the average more enriched in
δ18O than the fossil bovine teeth would support the
hypothesis that these Miocene boselaphines browsed
more and drank less while the fossil bovines grazed more
and as a consequence also drank more. However, this
argument is tenuous based on the current data. The most
enriched δ18O values are those of boselaphines while the
single most depleted value is from a bovine specimen
(Fig. 2A). Tooth enamel δ18O values show no consistent
relationship either to morphology or to locality. Rather,
the variation in δ18O values probably reflects behavioral
differences in water intake at the level of the different
individuals sampled. Living Bovini, Boselaphini, and
Tragelaphini are obligate drinkers more or less tied to
water sources, though much of their water intake must
derive also from the plant matter they ingest, and this
may have been the situation for their late Miocene fossil
relatives as well. Variations in enamel δ18O values can
be the result of any number and combination of water
intake behaviors such as feeding from canopy tops
(enriched) vs. understory (depleted), or drinking from
evaporating waterholes (enriched) vs. rivers (depleted).
These behaviors are likely to have been highly variable
even within individual bovids from place to place and
season to season. Thus, the late Miocene bovines and
boselaphines sampled appear to have been opportunistic
rather than restricted in their water intake behaviors.
5. Conclusions
Thirty fossil dental specimens attributable to late
Miocene (∼8 Ma) bovines and boselaphines were
sampled for bioapatite carbon and oxygen isotope
ratios. The results provide support for fine-scale nichepartitioning between these two bovid phylogenetic/
functional groups along a dietary axis reconstructed
using δ13C carbon isotope ratios. All values are clustered between −9‰ and −13‰, indicating that both
bovines and boselaphines lived in pure C3-dominated
environments. In accordance with predictions made on
the basis of the functional morphological differences
between fossil bovine and boselaphine teeth (Bibi,
2007), fossil bovine dental enamel on the whole exhibits
significantly more positive δ13C values while fossil
boselaphine teeth have more negative δ13C values. Enrichment of the heavier isotope of carbon (more positive
δ13C values) in bovine teeth is indicative of feeding on
C3 plants growing in more open environments–such as
canopy gap clearings or grasses in open C3 grasslands–
than inhabited by boselaphines which exhibited more
negative values signifying feeding in more closed
habitats. Outlier specimens within both the bovine and
boselaphine series indicate that while diets were on the
whole different, important dietary variations at the
individual level were often significant, resulting in some
more depleted and more enriched δ13C values than
expected in bovines and boselaphines, respectively.
Niche breadth, estimated as the variance of bovine and
boselaphine δ13C values about their respective means,
does not differ significantly between these two bovid
groups. There is thus no evidence here that the evolution
of novel morphological features associated with increased grazing permitted a broadening of the fundamental niche in early bovines. However, the fact that all
specimen δ13C values in this study are clumped at the
most positive end of the C3 feeding range gives reason
to consider whether the absence of a C4 component may
preclude detection of expanded niche breadth in this
case. Further studies including younger specimens
(b7.4 Ma) and the C4 dietary spectrum may better address the question of fundamental niche broadening.
Oxygen isotope δ18O values are not significantly
different between late Miocene bovines and boselaphines. Living representative of Bovinae (Bovini +
Boselaphini + Tragelaphini) are all obligate drinkers
more or less dependant on proximity to water bodies,
and it is likely that this was the case for both the fossil
bovines and boselaphines sampled in the study.
This study has utilized stable isotopes to test ecological hypotheses developed on the basis of functional
analysis of dental occlusal morphology (Bibi, 2007).
The result is a high-resolution analysis that discriminates between more closed- and more open-environment
resource use within a narrow range of isotopic values
F. Bibi / Palaeogeography, Palaeoclimatology, Palaeoecology 253 (2007) 529–538
(∼3‰). In tracing the morphological and ecological
origins and evolution of a single herbivorous clade
(Bovini), this study contributes to ongoing and wideranging efforts to reconstruct and explain the emergence
of proto-modern climate systems, biotas, community
structures, and taxa in late Miocene times, between
about 10 and 5 Ma.
Acknowledgements
I am most grateful to G. Olack for his help in running
the specimens at the Earth Systems Center for Stable
Isotopic Studies, Yale University. R. Feranec, L. Grawe,
and W. Straight provided much advice on sample collection and preparation. L. Grawe generously provided
me with samples of MEme standard. B. Tipple, R.
Ferance, M. Pagani, E. Vrba, and two anonymous
reviewers provided comments that much improved an
earlier draft of this manuscript. This work was supported
by a Yale Institute for Biospheric Studies Center for
Field Ecology grant, a Geological Society of America
Ross Research Award, and a National Science Foundation Graduate Research Fellowship.
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