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A high prevalence of enamel hypoplasia in several herbivores from the early Pliocene Langebaanweg locality, South Africa, indicates general systemic stress during the growing years of life. The presence of several linear enamel hypoplasias per tooth crown in many teeth further suggest that these stress events may be episodic. The delta18O values along tooth crowns of mandibular second molars of Sivatherium hendeyi (Artiodactyla, Giraffidae) were used to investigate the cause of the stress events in this tooth type. Results show that weaning in this fossil giraffid occurred at a similar ontogenetic age to that in extant giraffes, and that the observed enamel hypoplasia towards the base of this tooth type manifested post-weaning. Further, high-resolution oxygen isotope analyses across S. hendeyi third molars suggest that the entire development of defective tooth crowns occurred under conditions of increased aridity in which the cool, rainy part of the seasonal cycle was missing. The high prevalence of this defect in many herbivores suggests that climatic conditions were not favourable. This study reiterates the value of stable isotope analyses in determining both the behaviour of fossil animals and the environmental conditions that prevailed during tooth development.
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101
Keywords. Early Pliocene; enamel hypoplasia; Langebaanweg; stable isotopes; weaning behaviour
J. Biosci. | Vol. 28 | No. 6 | December 2003 | 101–000 | © Indian Academy of Sciences
Insights from stable light isotopes on enamel defects and
weaning in Pliocene herbivores
TAMARA A FRANZ-ODENDAAL
1,
*, JULIA A LEE-THORP
2
and ANUSUYA CHINSAMY-TURAN
1
1
Department of Zoology,
2
Department of Archaeology, University of Cape Town,
Private Bag Rondebosch, 7701, South Africa
*Present address: Department of Biology, Dalhousie University, 1355 Oxford Street, Halifax,
Nova Scotia, B3H 4J1, Canada
*Corresponding author (Fax, 902-494-3736; Email, tfranzod@dal.ca)
A high prevalence of enamel hypoplasia in several herbivores from the early Pliocene Langebaanweg locality,
South Africa, indicates general systemic stress during the growing years of life. The presence of several linear
enamel hypoplasias per tooth crown in many teeth further suggest that these stress events may be episodic. The
δ
18
O values along tooth crowns of mandibular second molars of Sivatherium hendeyi (Artiodactyla, Giraffidae)
were used to investigate the cause of the stress events in this tooth type. Results show that weaning in this fossil
giraffid occurred at a similar ontogenetic age to that in extant giraffes, and that the observed enamel hypoplasia
towards the base of this tooth type manifested post-weaning. Further, high-resolution oxygen isotope analyses
across S. hendeyi third molars suggest that the entire development of defective tooth crowns occurred under
conditions of increased aridity in which the cool, rainy part of the seasonal cycle was missing. The high pre-
valence of this defect in many herbivores suggests that climatic conditions were not favourable. This study
reiterates the value of stable isotope analyses in determining both the behaviour of fossil animals and the
environmental conditions that prevailed during tooth development.
[Franz-Odendaal T A, Lee-Thorp J A and Chinsamy-Turan A 2003 Insights from stable light isotopes on enamel defects and weaning in
Pliocene herbivores; J. Biosci. 28 000000]
1. Introduction
Towards the end of the Miocene major changes in global
climates and environments had profound effects on bio-
logical systems (Kurten 1972; MacFadden et al 1996;
Janis et al 2000). By the early Pliocene, climates had
become cooler, drier and more seasonal, with grasslands
expanding to replace the tropical and subtropical forests
characteristic of the Miocene (MacFadden et al 1996;
Cerling et al 1997). At the same time, grazers with hyp-
sodont dentition became more common in faunal assem-
blages (Janis 1993), including in the rich fossil assemblage
at the early Pliocene site of Langebaanweg, South Africa
(18°9E, 32°58S). The Langebaanweg assemblage includes
a diverse collection of artiodactyls, of which the extinct
giraffid, Sivatherium hendeyi, is most abundant. The
assemblage is unusual and unique. It is the only southern
African site in the latest Miocene/early Pliocene epochs
with a large assemblage of vertebrates, in which the in-
troduction of several new forms of larger vertebrates is
observed (Hendey 1984). That is, Langebaanweg is uni-
quely positioned at a time when Africa’s rainforests were
being replaced by grasslands, as a result of global climate
changes. Second, a developmental tooth defect known
as enamel hypoplasia was observed to be prevalent in
S. hendeyi specimens during early excavations (Hendey
1981). It was suggested that these defects were the result
of dietary stress related to the reduction of forest habitat
and expansion of C
4
grasslands, to which, it was assumed,
sivatheres were poorly adapted (Hendey 1981). According
to the C
4
global expansion model (Cerling et al 1997), C
4
grasses could have reached mid-latitudes in southern
J. Biosci. | Vol. 28 | No. 6 | December 2003
Tamara A Franz-Odendaal, Julia A Lee-Thorp and Anusuya Chinsamy-Turan
102
Africa by the early Pliocene. C
4
grasses had reached
similar latitude sites in South America by this time (Mac-
Fadden et al 1996), but carbon isotope evidence indicates
that Langebaanweg remained a C
3
dominated habitat
(Franz-Odendaal et al 2002). Hence, the high prevalence
of enamel hypoplasia observed in S. hendeyi cannot be
attributed to the C
3
C
4
grassland shift. This study shows
that enamel hypoplasia is present, not only in S. hendeyi,
but also in many other herbivores which were recovered
from the Langebaanweg locality, suggesting systemic
stress was experienced during the growing years of life
in a large cohort of animals. Based on δ
18
O values along
tooth crowns of second molars of S. hendeyi, we show
that weaning occurred at a similar ontogenetic age to that
in extant giraffes, and that enamel hypoplasia in this tooth
manifested itself post-weaning. In addition, high-resolution
isotope analyses across third molars suggest a link between
dental defects and a drier climate in which the cool, rainy
part of the seasonal cycle was missing.
Since enamel is not remodelled during life, it provides a
permanent non-specific record of events (mainly physio-
logical) that occurred during tooth development. Linear
enamel hypoplasia is caused by a disruption in ameloblasts
that lay down the enamel matrix (Goodman and Rose 1990),
resulting in defects. These defects manifest as a linear
arrangement of pits or horizontal grooves across the tooth
surface (figure 1). Systemic stress episodes that occur at
a particular ontogenetic age affect all teeth developing at
the time of the stress. Linear enamel hypoplasia has been
linked to nutritional stress (Neiburger 1990; Goodman
and Rose 1991; Dobney and Ervynck 2000), birth stress
(Goodman and Rose 1991; Mead 1999), weaning stress
(Goodman and Rose 1991; Dobney and Ervynck 2000),
and stress associated with calf-cow separation (Mead
1999). Stress must reach a threshold level before amelo-
blasts are disrupted and a linear defect is manifested
(Goodman and Rose 1990).
Thus, the presence of these defects in a population can
provide a unique perspective into prevailing environmental
conditions by indicating the health status during the early
(growing) years of life. Few occurrences of linear enamel
hypoplasia have been reported in non-primate fossil
animals (Mead 1999; Dobney and Ervynck 2000; Niven
2002), yet analyses of this defect remain both a powerful and
popular tool in anthropology (Goodman and Rose 1990).
2. Materials and methods
To investigate whether defects correlated with particular
diets (i.e. nutritional stress), we first determined the extent
of enamel hypoplasia in the Langebaanweg faunal assem-
blage. We examined almost 3000, mostly isolated, teeth
from herbivores forming part of the large and diverse
collection of vertebrate fossils from the fluviatile deposit
(pelletal phosphate member) at Langebaanweg. The position
and size of each defect was recorded and measured with digi-
tal callipers. Tooth hypoplastic area (THA) scores (after En-
sor and Irish 1995), indicating the percentage of total crown
height that is defective, were calculated for each animal.
Using stable oxygen isotope ratios from enamel apatite
carbonate, across defective tooth crowns, the timing and
seasonality of the occurrence of these defects was estab-
lished. All stable isotope values are reported relative to the
PeeDee Belemnite standard in parts per mil (‰). Only
unworn or very slightly worn teeth were selected for serial
isotope analyses, and on an average, twelve samples were
obtained per tooth crown. Serial samples were drilled in
thin horizontal grooves ~ 1 mm apart across the entire
tooth crown, from top to base. This approach enabled us
to make some inferences about the cause of the observed
stress episodes. It also provided us with fresh insight into
the environmental conditions that prevailing at the time.
However, this approach has a drawback. Defects occur
during the initial laying down phase of enamel, whereas
apatite development and, hence, incorporation of carbonate
proceeds from this point onwards until the end of minera-
lization. In domestic sheep, for example, three waves of
mineralization occur (Suga 1982). Hence a defect at a cer-
tain position on the tooth crown represents a stress episode
that occurred during the initial secretion of enamel pro-
tein, but the
18
O/
16
O composition reflected at that point
on the crown represents an accumulation of the isotope sig-
nal throughout the process of amelogenesis.
3. Results
An investigation of ~ 2000 mandibular teeth belonging to
S. hendeyi showed that deciduous teeth were unaffected
by linear enamel hypoplasia, whereas all permanent teeth
had defects (Franz-Odendaal et al 2003). This finding
indicates that throughout development of the adult denti-
tion [which in extant giraffes commences pre-birth and
ends at around 56 years (Hall-Martin 1976)], unfavou-
rable and stressful conditions were experienced. Further-
more, 35% of S. hendeyi teeth have more than one defect
on an individual tooth crown suggesting that stress epi-
sodes were also episodic. The distribution, incidence and
size of linear defects in each tooth type are variable (Franz-
Odendaal et al 2003) and suggest that the duration of the
stress episodes varied at different times during ontogeny.
By extending this analysis to other herbivores, our results
show that linear enamel hypoplasia is not confined to
S. hendeyi but is present in almost all the herbivores from
the Pelletal Phosphate Member at Langebaanweg (figure 2).
Several distinct linear defects were observed in the conti-
nually erupting hippopotamus tusks, indicating that stress
episodes were not confined to the developing years of an
animal’s life but that they also extended into adulthood.
J. Biosci. | Vol. 28 | No. 6 | December 2003
Enamel hypoplasia in Pliocene herbivores
103
The highest incidence of linear enamel hypoplasia
(> 20%) was observed in the hippopotamus (Gen. and sp.
undet.), sivathere (S. hendeyi), and reduncines (Kobus
sp.). The duration of the stress episodes (i.e. the width
of each defect) is reflected by the THA score for each
animal. Average scores indicate that the hippopotamus
Figure 1. Hippopotamus teeth with linear enamel hypoplasia. (A
) Tusk fragment (SAM
PQL 58905), with several linear de
fects, the dashed vertical line indicates a wide band of
pits whereas the other three defects (arrows) are fairly narrow. (B)
Incisor fragment (SAM
PQL 51371), dashed vertical lines indicate areas with linear grooves. (C
) Tusk (SAM
PQL 58973), dashed line indicates the width of a linear defect. Scale bars represent 1
cm.
Sample accession numbers are from the South African Museum, Cape Town.
J. Biosci. | Vol. 28 | No. 6 | December 2003
Tamara A Franz-Odendaal, Julia A Lee-Thorp and Anusuya Chinsamy-Turan
104
and reduncine were most severely affected (with scores
greater than 35%).
4. Discussion
4.1 Enamel hypoplasia and nutrition
Nutritional stress is the most commonly reported cause
for linear enamel hypoplasia (Goodman and Rose 1990).
From
13
C/
12
C analysis, we were unable to determine
whether the incidence of defects correlated with dietary
preference because of the C
3
-dominant environmental
signature at Langebaanweg (Franz-Odendaal et al 2002).
Instead, we compared the fauna with their modern relatives
or to similar species at other localities in Africa of a
similar age. Conservative diets within fossil and extant
Hippopotamidae (Bocherens et al 1996; Zazzo et al 2000)
and Alcelaphinae (Damalacra sp.) (Zazzo et al 2000) sug-
gest that these animals were almost exclusive grazers in
North and East Africa from ~ 5 Mya. Although the diets
of fossil Giraffidae were probably highly heterogeneous
(Solounias et al 2000),
13
C/
12
C analysis of Giraffa jumae
at the Pliocene site of Makapansgat (South Africa) has
confirmed that this species was a browser (Sponheimer
et al 2003). Giraffa cf. jumae is present at Langebaanweg.
Both the Palaeotraginae and Sivatheriinae had grazing,
mixed feeding and browsing members during the Mio-
cene epoch (Solounias et al 2000) and their diets at
Langebaanweg remain uncertain. The boselaphine (Mesem-
brioportax acrae) was assumed to be a browser (Hendey
1983b). Data from other localities in Africa indicate that
the reduncine (Kobus sp.), rhinoceros (Ceratotherium prae-
cox) and bovine (Simatherium demissum) from this loca-
lity were either mixed feeders or grazers (Sponheimer
et al 1999, 2001; Zazzo et al 2000). Our results indicate
that animals that eat grass, such as hippopotamuses and
alcelaphines (Damalacra sp.), are not equally affected
with enamel hypoplasia defects, indicating that there
is not a simple correlation between prevalence of linear
Figure 2. Linear enamel hypoplasia (LEH) in herbivores from the pelletal phosphate deposit, Lang
e-
baanweg, South Africa. Open bars represent the percentage of teeth affected with LEH
(i.e. incidence);
closed bars represent the percentage of tooth crowns affected which has been expressed as an aver
age for
the animal (i.e. average THA scores for each animal). Presumed browsers are on the left, expected gra
z-
ers on the right
, and animals with uncertain dietary habits in the middle. The sum of the widths of each
defect on a tooth crown was divided by the crown height of each defective tooth, to give a THA score.
Average scores for each animal were then calculated. Fragmented t
eeth were excluded from the analysis
except for the hippo where large tusk fragments were included. Numbers in parenthesis indicate the nu
m-
ber of permanent teeth analysed. Giraffids include Giraffa cf. jumae (259), Palaeotragus cf.
germaini
(24) and the sivathere S. hendeyi (1544). Other animals include the boselaphine Mesembiportax
acrae
(152), reduncine Kobus sp. (42), the rhinoceros Ceratotherium praecox (41), the alcelaphine
Damalacra
sp. (191), the bovine Simatherium demissium (116) and the Hippopotamidae (Gen and sp. undet.) (196).
J. Biosci. | Vol. 28 | No. 6 | December 2003
Enamel hypoplasia in Pliocene herbivores
105
enamel hypoplasia and diet. Another cause for the sys-
temic stress underlying the occurrence of these defects
must exist. Differences in the prevalence of linear defects
between taxa with similar diets may relate to differences
in behaviour and/or tolerance levels for stressful condi-
tions.
4.2 Enamel hypoplasia and weaning
Amongst the ~ 2000 Sivatherium teeth examined, only
the upper third of the m1 is devoid of defects (Franz-
Odendaal et al 2003) and since this tooth begins develop-
ment before parturition, this portion of the tooth crown
perhaps corresponds to a stress-free in utero period. In
extant giraffes, it is well documented that weaning is ref-
lected primarily in the later development of the m1
and
in the earliest development of the m2, but the onset and
duration of weaning varies greatly depending on the qua-
lity of available vegetation (Hall-Martin 1976). It is, how-
ever, not certain whether modern giraffes provide reasonable
analogues for the timing of tooth development and wean-
ing in extinct sivatheres. In an effort to ascertain when, in
tooth ontogeny, weaning occurred in S. hendeyi, and whe-
ther the subsequent stress episodes were linked to seasonal
changes, we turned to high-resolution intra-tooth
18
O/
16
O
sequences.
Both enamel phosphate (PO
4
) and carbonate (CO
3
)
δ
18
O closely reflect body water δ
18
O, although absolute
α
bw-PO4
and α
bw-CO3
differ. Serial analyses from top to
base of the tooth crown reflect seasonal changes during
tooth development in modern and fossil animals (Koch
et al 1989; Bryant et al 1994; Fricke and O’Neil 1996;
Stuart-Williams and Schwarcz 1997; Feranec and Mac-
Fadden 2000; Balasse et al 2002). The weaning transition
is detectable because milk is significantly enriched in
18
O
compared to drinking water, resulting in higher δ
18
O
CO3
in suckling calves compared to weaned calves and adults
(Fricke and O’Neil 1996).
In the extant giraffe, relatively higher δ
18
O values,
reflecting suckling, were observed in the uppermost portion
of an unworn m2 (figure 3A, arrow) as expected from
their weaning behaviour (Hall-Martin 1976). Four out of
five of the sivathere m2s have similar higher δ
18
O values
(figure 3B) indicating that, in most individuals, weaning
was completed during development of the top of the
tooth crown. Hence weaning in S. hendeyi occurred at
a similar ontogenetic period to extant giraffes. Defects
towards the base of the m1 (Franz-Odendaal et al 2003)
might be associated with weaning as in humans (Goodman
and Rose 1990) and pigs from archaeological sites (Dobney
and Ervynck 2000), but linear defects present in the rest
of the permanent dentition cannot be attributed to this
particular systemic stress.
4.3 Enamel hypoplasia and climate
The clearest isotopic indicators of seasonal cycles are
archived in the third molars (Fricke and O’Neil 1996),
which develop well after weaning in giraffes (Hall-Mar-
tin 1976). To investigate whether defects were correlated
with seasonality regime, we obtained a high-resolution
δ
18
O series from three normal and three defective S. hen-
deyi m3s (figures 4 and 5). Serial δ
18
O
enamel
measure-
ments on modern and archaeological sheep and cattle
from this area of South Africa showed seasonal cyclicity
in which the cool, wet winter is recorded as low δ
18
O
values while the dry summer season values are higher
(Balasse et al 2002). A similar cyclical pattern is obser-
ved in the sivathere normal teeth with seasonal amplitudes
of more than 2‰ (figure 4). In m3s with linear enamel
hypoplasia seasonal amplitude is reduced, mostly because
the lower δ
18
O (winter/rainy season) part of the cycle is
missing (figure 5). The lowest seasonal amplitude of
09‰ occurs in tooth SAM PQL 62733/62 which has the
broadest defect affecting over 36% of the tooth crown
(figure 5A). In tooth SAM PQL 62733/61, seasonal
amplitude is low (09‰) in the area with three narrow
defects, while it is 17‰ in the broad basal portion of this
tooth (figure 5B), which is similar to normal teeth. The
pattern is less similar for tooth SAM PQL 62733/13, where
a negative δ
18
O shift corresponds with a linear enamel
hypoplasia at the base of the tooth (figure 5C); neverthe-
less the seasonal pattern differs from that of the normal
teeth. The results suggest that defective enamel co-occurs
with a significant reduction in the overall seasonality,
in which the wet season (winter) is completely or partly
missing. Although several defects on a tooth crown sug-
gest episodic stress event(s) interspersed with favourable
conditions, these results suggest that development of the
entire crown occurred under conditions of increased ari-
dity or drought. The possibility that altered chemistry
in defective areas could produce these differences in
δ
18
O is remote, since the defects manifest in the organic
template and infrared microscopy shows the standard
enamel apatite structure (figure 6).
It has been suggested that a strongly seasonal rainfall
regime existed at Langebaanweg 5 Mya (Hendey 1983a),
based on pollens (Scott 1995) and taphonomic context that
suggests flood episodes (Hendey 1981). The δ
18
O series
for the six S. hendeyi m3s suggest two kinds of climate
scenarios one in which there were regular wet seasons,
expected seasonal amplitudes, and no enamel hypoplasia,
and the other where the wet season is missing, seasonal
amplitude is low, and defects become prevalent. The latter
suggests drier conditions. The inference that the stress
agent was aridity is also supported by the distribution
of stressed animals. The hippopotamus and reduncines,
both of which are extremely water-dependant today, have
J. Biosci. | Vol. 28 | No. 6 | December 2003
Tamara A Franz-Odendaal, Julia A Lee-Thorp and Anusuya Chinsamy-Turan
106
the highest incidence and average THA scores (figure 2).
Probable browsers (Giraffa sp. and boselaphine) also
have fairly high THA scores, indicating that not only was
available drinking water limited but that the water con-
tent of browse was also reduced. Known grazers (e.g.
Damalacra sp.) that would have been less dependent on
water and possibly migratory have the lowest scores.
The large-scale climate changes at the end of the Mio-
cene/early Pliocene placed many herbivores previously
adapted to warmer, wetter and more stable environmental
conditions, under stress (as noted by, for example, Janis
1993). Some of these lineages would have been able to
adapt relatively quickly to the changing climatic conditions.
Our results suggest that climatic conditions on both a large
Figure 3. Stable oxygen isotopes along lower second molars. (A) Extant giraffe, Giraffa camelopa
r-
dalis, and (B) the extinct giraffid, S. hendeyi, showing similar enriched δ
18
O values near the top of the
tooth crown (arrows). Y-axis indicates direction of tooth deve
lopment from top of the crown towards the
base (0 mm).
(A)
(B)
J. Biosci. | Vol. 28 | No. 6 | December 2003
Enamel hypoplasia in Pliocene herbivores
107
and small time-scale (i.e. during the life of an individual)
were highly variable. The high incidence of enamel hypo-
plasia linked to frequent drought episodes suggests that
these highly variable climatic conditions were new to ani-
mals living in the late Miocene/early Pliocene, and that many
of the animals (particularly those dependent on drinking
water) suffered as a result. The unique (geographical and
chronological) position of Langebaanweg, right at the
time when global climates were changing, enables us to
gain insight into the prevailing environmental conditions
and their effects on terrestrial fauna. The only other site
in southern Africa containing large vertebrate fauna in
roughly this time period is located in the site of Sterkfon-
tein, almost 50 km to the northwest of Johannesburg, in
the interior of South Africa. The age of Member 2 and the
Jacovic Cavern has been estimated to be about 42 Mya
from cosmogenic nuclide and palaeomagnetic dating (Par-
tridge et al 2003). Although several hominids, not yet
identified to species, have been discovered in Member 2
and the Jacovic Cavern, only the latter reportedly contains
a range of large vertebrates (Partridge et al 2003).
5. Conclusions
Our results indicate a correlation between the presence of
linear enamel hypoplasia in a large early Pliocene faunal
assemblage and reduced seasonality (aridity) in Southern
Africa. These adverse climatic conditions persisted from
development and throughout adulthood, and placed seve-
ral herbivores under severe systemic stress that ultimately
resulted in the manifestation of linear enamel hypoplasia.
Figure 4. Stable oxygen isotopes along normal lower th
ird
molars of S. hendeyi. Y-axis indicates direction of tooth deve
l-
opment from top of the crown towards the base (0
mm) and
the x-
axis indicates wetter/cooler (left) to drier/warmer (right)
en
vironments. One data point (in tooth SAM PQL 62733/16)
could not be determined conclusively.
Figure 5. Stable oxygen isotopes along lower third molars of S
hendeyi with linear enamel hypoplasia. (A
(B) SAM PQL 62733/61, and (C) SAM PQL 62733/13. The pos
tion of the defects on each tooth is indicated with arrows. (A
one broad defect, (B) has three narrow defects and (C
medium-
explanation of the axes refer to figure 4.
(A)
(B)
(C)
Figure 6. Fourier transform infrared spectroscopy of nor
mal
and defective S. hendeyi
enamel, SAM PQL 43928 and SAM
PQL 44053 respectively. The position and ampli
tude of peaks is
characteristic of different kinds of apatites (
LeGeros 1981,
1991; Sponheimer and Lee-Thorp 1999). The character
istic
enamel apatite pattern (Sponheimer and Lee-
Thorp 1999) is
found in both defective and normal S. hendeyi
enamel from
Langebaanweg, South Africa.
J. Biosci. | Vol. 28 | No. 6 | December 2003
Tamara A Franz-Odendaal, Julia A Lee-Thorp and Anusuya Chinsamy-Turan
108
In addition, we show that high-resolution isotope analyses
can provide otherwise unobtainable insights into the wean-
ing behaviour of extinct animals and can be used as a tool
to understand the environmental contexts under which
developmental dental disease manifests.
Acknowledgements
The National Research Foundation and the University of
Cape Town funded this study. We thank D Ohland (Head
of Research and Collections, South African Museum) and J
Lanham (Stable Light Isotope Facility, University of Cape
Town, SA) for their assistance, and two anonymous review-
ers for comments on an earlier version of this manuscript.
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MS received 7 January 2003; accepted 3 September 2003
Corresponding editor: DOMINIQUE G HOMBERGER
... The ridges between the grooves denote a temporary return to more normal growth conditions. Enamel hypoplasia has been observed in teeth of many mammalian species, including the maxillary and mandibular canines of hippopotamids (Dietrich 1928;Matthes 1939;Kuss 1957;Franz-Odendaal et al. 2003). The occurrence of this developmental defect was linked to systemic stress caused by environmental or animal-related factors, including nutritional deficiencies, intoxication, disease, birth and weaning (Goodman and Rose 1990;Mead 1999;Dobney and Ervynck 2000;Franz-Odendaal et al. 2004;Witzel et al. 2008;Hillson 2014). ...
... According to Mead (2000), the habitat requirements of Teleoceras were similar to those of the extant African Hippopotamus amphibius. Franz-Odendaal et al. (2003) found a high prevalence of linear enamel hypoplasia in teeth of hippopotamids (genus and species indet., most likely Hexaprotodon) from the Lower Pliocene site of Langebaanweg (South Africa). The finds include tusk fragments showing transverse hypoplastic enamel defects of different width, including one specimen with a broad defect resembling those present in the two canine fragments of the Untermassfeld hippos. ...
... This stress could have been caused by repeatedly occurring adverse environmental conditions� A possible scenario would be periodic nutritional limitation related to seasonal variation in plant growth (dry periods?). If this scenario can be substantiated by further palaeoenvironmental studies at the Untermassfeld site, it would form an interesting parallel to the findings of Franz-Odendaal et al. (2003) on hippopotamids from the Lower Pliocene site of Langebaanweg, South Africa. It would also mean that the Untermassfeld hippos probably had to walk longer distances during the period of reduced food availability to meet their nutritional requirements. ...
... On the basis of ease of enamel examination, sensitivity, failure to remodel, and chronological array of its developmental pattern it can be the perfect tissue for recording alterations in physiology of an animal during its tooth development (Kreshover, 1940;Massler et al., 1941;Sarnat & Schour, 1941). The indications of EH in fossilized material, especially in mammalian dentition, has been recently unveiled by many paleontologists (Mead, 1999;Franz-Odendaal et al., 2003, 2004Franz-Odendaal, 2004;Byerly, 2007;Roohi et al., 2015;Bohmer & Rossner, 2017;Ahmad et al., 2018;Barron-Ortiz et al., 2019), which add an additional and much reliable evidence to propose the paleoclimatic fluctuations on regional scale. Physical anthropologists frequently study the defects of tooth enamel to assess the frequency of physiological stressors including mineral deficiencies, metabolic disruptions, premature births, and contagious diseases (Pindborg, 1982). ...
... The perturbations of EH occur as a result of three causal situations: (i) localized trauma, (ii) hereditary anomalies, or (iii) physiological or systematic metabolic stress (parturition, weaning, nutritional, illness and stress during cow-calf separation) in developing teeth at a specific ontogenetic age (Weinmann et al., 1945;Shawashy & Yaeger, 1986;Suckling, 1989) recognized as EH (Goodman & Rose, 1990;Neiburger, 1990;Mead, 1999;Dobney & Ervynck, 2000;Lukacs, 2001;Franz-Odendaal et al., 2003). The perturbations resulting as hereditary causes are the most severe and usually affect all of an animal's teeth (Weinmann et al., 1945;Stewart & Poole, 1982). ...
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The paleoecological fluctuations left their impression marks on the tooth enamel of mammals during their tooth development. These marks can be used as stress indicators because they reflect the type of duress faced by the extinct mammalian species during their lives. The enamel hypoplasia (EH) is a common stress marker to trace out the paleoenvironment of the region and the likelihood of species extinction. The material used for current EH analysis belongs to the genus Deinotherium, family Deinotheriidae, collected from Middle Miocene (15.2–11.2 Ma) Siwaliks of Pakistan. In this analysis 35 samples consisting of 52 teeth of two species, Deinotherium pentapotamiae and D. indicum, are included. The results indicate that 13/52 (25%) of the analyzed teeth have occurrences of EH giving a prediction that these Siwalik deinotheriids were facing the physiological and/or ecological stresses during the Middle Miocene epoch of Pakistan. The higher frequency of EH in molars (30.30%) compared to premolars (21.05%) express that the individuals experienced a comparatively high stress at the adult stages of their lives. This higher magnitude of EH in molars supports the idea of ecological stressors, i.e., dietary, mating, disease, and predator-prey associations, amplify the likelihood of extinction by dint of EH occurrences.
... As regards stable oxygen isotopes from the archaeological assemblage, due to the presence of both worn and unworn molars which cannot be precisely identified (M1/3), it is possible that at least in some teeth the results are influenced by the lactation signal, reflecting in M1 the composition of mother's body water rather than that of meteoric water (Fricke and O'Neil 1996;Franz-Odendaal et al. 2003;Henton et al. 2010). However, the contiguous maxillary molars TDB-4 (M1/2) and TDB-5 (M2/3) are particularly promising to observe the isotopic composition of cattle water intake over a long period, as these teeth represent the longest time span observable for an individual cow in the dataset obtained. ...
... As a confirmation, the series TDB-4/TDB-5, formed over at least one year, never reaches values higher than − 7.7‰. The potential impact of lactation on the data could not fully explain this anomaly, as it would have probably resulted in slightly higher pre-weaning values (Fricke and O'Neil 1996;Franz-Odendaal et al. 2003), due to the presence of δ 18 Oenriched plant water in cow's milk (Camin et al. 2008). ...
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Tana del Barletta is an upland cave used from the Late Neolithic to the Middle Bronze Age, located in the vicinity of the coast in Liguria (NW Italy). The excavation revealed the presence of a faunal assemblage dominated by caprine and cattle remains. In order to gain new data on late prehistoric farming strategies (e.g. seasonal mobility, coastal grazing, animal diet), intra-tooth series of stable oxygen and carbon isotopes have been obtained from cattle and sheep/goat tooth enamel, along with intra-tooth series of nitrogen and carbon isotopes from cattle dentine collagen. Due to the prevalence of maxillary teeth, a modern calf has also been analysed to assess intra-individual isotopic differences between the maxillary and mandibular dentition. Modern data on oxygen isotope values of meteoric water from different altitudes around the area of the site were used as a reference for interpretation. The results indicate that the water ingested by the herd was mostly characterised by particularly low δ ¹⁸ O values, highlighting the importance of the uplands for the late prehistoric farmers of the region. However, the input of water sourced from lower elevations, especially during the winter months, cannot be dismissed. In addition, the nitrogen isotopic composition of cattle collagen rules out the ingestion of salt-tolerant vegetation or seaweed, suggesting that grazing did not occur directly on the coastal plain.
... Most herbivorous mammals have hypsodont dentition which is characterized by high-crowned teeth, and offer an opportunity for a higher resolution for BWP reconstruction because of the relatively elongated enamel. Franz-Odendaal et al. (2003) Bryant et al. (1996a) constructed a mass balance model incorporating seasonal fluctuation, enrichment through breast milk intake, and the effect of body growth on equid enamel d 18 O values, and concluded that the patterns of d 18 O change among different teeth types were attributed to different birth seasons. Based on this result, they showed that the most equid individuals were born in spring for Miocene equids from Nebraska (Bryant et al., 1996a) and Eocene-Oligocene equids from Wyoming and South Dakota (Bryant et al., 1996b). ...
... Thus, nitrogen isotope analysis on organic components is fairly difficult for the reconstruction of BWPs in hominins and other mammalian species that lived before a few ten thousands of years ago. Oxygen isotope analysis (Franz-Odendaal et al., 2003) and trace element analysis (Austin et al., 2013) would be helpful in estimating the weaning ages of such ancient species. ...
Chapter
In Japan, the populations of most urbanized cities decreased during the middle to late premodern period (eighteenth–nineteenth century). The cities of Osaka and Kyoto experienced major population decreases, one of the causes of which is assumed to be the persistently high proportion of live-in servants present. Historical demographic analyses indicated that this hoko-type employment led to an older age at first marriage and lower fertility. In this study, the ages at the end of weaning in urban areas adjacent to Osaka and Kyoto were reconstructed by measuring stable isotope ratios of subadult skeletons. The reconstructed age at the end of weaning (1.9 and 2.4 years) was younger than that in typical premodern populations in Japan (~3 years). Such younger ages at the end of weaning would have led to shorter inter-birth intervals and probably alleviated the negative effect of a higher proportion of hoko-type employment on fertility. Although this study exhibits some historical and bioarcheological limitations and suffers from a small sample size, we argue that the estimated earlier age at the end of weaning in these cities might have been a result of an increased need for heirs in the inheritance-based family system under the conditions of an older age at first marriage in premodern urbanized cities in Japan.
... Enamel hypoplasia has been widely studied in primates and especially in humans (Ogilvie et al., 1989;Goodman & Rose, 1990;Lukacs, 1999;Franco et al., 2007;Skinner & Pruetz, 2012;Cabec et al., 2015;McGrath et al., 2018), but it has been reported and investigated in many other mammal groups (pigs: Dobney & Ervynck, 2000; sheep and goats: Kierdorf et al., 2012;giraffes: Franz-Odendaal et al., 2004;bisons: Niven et al., 2004;rhinoceros: Bratlund, 1999;Mead, 1999;Fourvel et al., 2015;Bacon et al., 2018). More than a hundred causes have been proposed in humans (Small & Murray, 1978), but the most commonly proposed in the literature are: nutritional stress (Goodman & Rose, 1991;Barrón-Ortiz et al., 2019), seasonality (Franz-Odendaal et al., 2003;Skinner & Pruetz, 2012;, weaning or cow-calf separation (Goodman & Rose, 1990;Mead, 1999;Dobney & Ervynck, 2000), birth (Mead, 1999;Niven et al., 2004;, and diseases (Bratlund, 1999;Rothschild et al., 2001). ...
... Such morphology of enamel hypoplasia (in contrast with the morphology of adjacent lines within the same tooth), suggests a greater intensity of the stressor, or the interaction of two or more factors (Goodman and Rose, 1990). That might be consistent with the long dietary and behavioral transition of the weaning, known to be one of the most stressful periods in various large-bodied mammals (Mead, 1999;Dobney and Ervynck, 2000;Franz-Odendaal, 2003;Franz-Odendaal et al., 2004;Niven et al., 2004;Witzel et al., 2006). ...
Article
The Coc Muoi fauna provides a good example of the type of tropical mammalian communities that existed in northern Vietnam during the late Middle Pleistocene. The first results of the analysis of hypoplasia indicated that rhinoceroses and wild cattle were exposed to multiple physiological and psychological stress events specific to age [Bacon et al., 2018. A rhinocerotid-dominated megafauna at the MIS6-5 transition: The late Middle Pleistocene Coc Muoi assemblage, Lang Son province, Vietnam. Quat. Sci. Rev. 186, 123–141]. In this paper, we aim to supplement the study of hypoplasia in the orangutans (Pongo) from Coc Muoi and, more widely, from different Pleistocene faunas. To address this issue, we conducted a macroscopic analysis of linear enamel hypoplasia [LEH] on Pongo from three collections: Coc Muoi (148–117 ka), Duoi U'Oi (70–60 ka), and Tham Khuyen (>475 ka). Such comparative analysis based on isolated teeth is constrained by numerous biases including: the small datasets; the differential representation of tooth types; the difficulty in distinguishing first from second molars; the small number of individuals [MNI]; the differential representation of males versus females. The data analysis has been divided into two parts: (1) an analysis of the frequency and expression of LEH on incisors, premolars, and molars (three sites), and (2) an analysis of the frequency and expression of LEH on a set of canines (Tham Khuyen). We used a reference sample composed of 17 adult and 10 immature Pongo individuals to determine the age range of fossil Pongo individuals, at the time of the defects. Results show that hypoplasia was a common phenomenon in Pleistocene Pongo: two individuals at Coc Muoi; 2 out of 3 individuals at Duoi U’Oi; and 4 out of 6 individuals at Tham Khuyen. They experienced multiple stresses between ∼2 and 5 years of age, a period of great vulnerability for immature individuals. The occurrence of accentuated lines of hypoplasia on canine crowns of Tham Khuyen suggests a greater intensity of the stressor, in a time range consistent with the long dietary and behavioral transition of the weaning. In terms of paleoecology, Pleistocene orangutans from the Asian mainland could survive in different environmental conditions than those they occupy today. Various sources (archaeozoology, geological context, and ecology of wild populations), suggest that they might have been larger apes than extant orangutans, living in limestone forests on hills and tower karsts.
... LEH formation and its relation to stable isotopes was the purpose of several pieces of research. Franz-Odendaal et al. (2003) analyzed LEH and enamel δ 18 O level in the teeth of Pliocene herbivores to assess age at weaning and climatic conditions in which they lived. ...
Article
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Objectives The aim of this paper is to assess linear enamel hypoplasia (LEH) on canines of adults from early modern Wroclaw cemeteries to compare δ¹³C and δ¹⁸O values in enamel formed before, during and after LEH formation, and to attempt to find a link between the selected indicators of the weaning process. Material and Methods 15 permanent canines with visible LEH were selected for analysis. Age at LEH formation was estimated using the Reid and Dean method. The perikymata count was used to estimate the duration of LEH formation. Incremental stable oxygen and carbon isotopes analysis was performed on tooth enamel to infer stress related to weaning and dietary patterns. Kruskal-Wallis ANOVA, Mann-Whitney U test and Spearman correlation were used in statistical inference. Results The average age of LEH formation was 3.14 years, with an average duration of 111 days. Stable carbon isotope values consistently increase in 73% of the individuals sampled. The values of δ¹⁸O do not show a dominant pattern. The average value of δ¹³C increases over the time of enamel formation. The δ¹³C values collected below LEH were negatively correlated with δ¹⁸O values and the duration of LEH termination. Conclusions Marking of carbon and oxygen isotopes indicates different stages of weaning. Advancements in diet change (determined by higher δ¹³C) corresponds with faster recovery after physiological stress episode. There is no evidence for different breastfeeding models between distinct parishes in early modern Wroclaw.
... Keeping in view all these facts EH has been used by different researchers as a credible stress marker for different extinct mammalian groups i.e. Pleistocene hominids (Molnar and Molnar, 1985), Pleistocene Neanderthals (Trinkaus, 2018), early Miocene primates (Lukacs, 2001), early Pliocene grazers and browsers (Franz-Odendaal et al., 2003), Pliocene giraffids (Franz-Odendaal et al., 2004), Miocene rhinocerotids (Mead, 1999;Böhmer and Rössner, 2018), Siwalik rhinocerotids (Roohi et al., 2015), Siwalik giraffids (Ahmad et al., 2018). There is no report about occurrence of EH in any extinct tragulid species from the Neogene or Quaternary deposits globally even though these are ecologically significant ungulates. ...
Article
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The present paper is the first ever report on occurrence of enamel hypoplasia in extinct tragulids. The dental defect, enamel hypoplasia is caused by suppressed function of enamel forming cells called ameloblasts. It is used as a reliable stress marker in different extinct mammalian taxa to trace out the level of ecological stress faced by these animals during their life histories. We have studied this defect in three extinct Siwalik tragulid species including; Dorcabune anthracotherioides, Dorcatherium majus and Dorcatherium minus. To assess habitat stability for the Neogene tragulids, dental remains from the middle Miocene-early Pliocene, ca. 13.5-4.0 Ma outcrops of the Siwalik of Pakistan were analyzed for the occurrence of linear enamel hypoplasia. According to our results there was a lower occurrence of enamel hypoplasia (13%) in the tragulid fossils from the middle Miocene outcrops (13.5-11.2 Ma) as compared to the late Miocene to the early Pliocene (11.2-4.0 Ma) tragulid remains (48%) which is statistically significant (p<0.05). The middle Miocene in the Siwaliks is hypothesized to have had warm and humid climatic conditions with dominance of dense forests whereas in the late Miocene to the early Pliocene there was a shift in the ecological conditions, with grasslands expanding at the expense of forests and woodlands and the climate gradually becoming less warm and humid. The current enamel hypoplasia results indicate that warm and humid dense forests were the preferred habitats for extinct tragulids present during the middle Miocene in the Siwaliks.
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Middle Miocene deposits at Maboko Island in the Nyanza Rift of Western Kenya (~15–14 Ma) have yielded a rich fossil mammalian record that documents a mid-Miocene faunal shift. Palaeoecological proxies for Maboko have previously been interpreted to indicate heterogeneous habitats, ranging from grassland to closed canopy forest and implicated in this turnover. Stable carbon and oxygen isotope data of fossil herbivore enamel from catarrhine-bearing deposits at Maboko were analyzed to reconstruct the nature of C3 vegetation (i.e., water-stressed or subcanopy), as well as determining if any C4 biomass, representative of more open woodland or grassland habitats, were consumed. Taxa sampled include representatives of ruminants, suoids, rhinocerotids, and proboscideans. δ¹³Cenamel and δ¹⁸Oenamel values of Maboko fossil herbivores indicate foraging strategies consistent with a C3 dominated ecosystem, exhibiting a range of δ¹³Cenamel signatures similar to those of extant browsing herbivores foraging in mosaics of open forest/woodland habitats. Within the Maboko sequence, isotopic evidence indicates alternating environments based on variable dietary spectra associated with discrete fossiliferous units within the succession. Relative to other stratigraphic beds, isotopic signals of herbivore enamel from Bed 5b, for example, reflect more closed woodland/forest foraging. The overall ~4‰ range of δ¹³Cenamel values from Maboko (−14.1‰ to −10.2‰) is statistically similar to δ¹³Cenamel values from the slightly younger middle Miocene site of Fort Ternan and is consistent with faunal and paleosol evidence from Maboko suggesting ecological variability. However, the isotopic evidence from Maboko indicates that environmental variability is more constrained than previously reconstructed, instead ranging from more open canopy forest to open woodland habitats, albeit with some spatial and temporal heterogeneity. Closed canopy forest plants and C4 biomass were not detectable as dietary components for any herbivores sampled thus far; nor was there evidence of significantly water-stressed C3 vegetation (possibly C3 grasses) being consumed.
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New δ13C values are presented for tooth enamel of 65 herbivorous fossil mammal specimens from low- and middle-elevation localities in Argentina ranging in age from Deseadan (ca. 27 Ma) to Lujanian (potentially as young as ca. 10,000 yrs BP). Prior to the Huayquerian (late Miocene; 9-6.5 Ma), all faunal levels have mean δ13C values of about -11 ± 1‰, indicating ancient terrestrial ecosystems with predominantly C3 plants. During the late Miocene through Pleistocene (i.e., after ca. 8 Ma), there is a statistically significant carbon isotopic shift so that: (1) taken together, later faunal levels have a combined mean δ13C value of -7.6‰ and (2) the data set includes significantly larger ranges of δ13C values (i.e., individual specimens are as positive as ca. +1‰). These post-8 Ma data indicate isotopically mixed terrestrial plant communities containing a significant component of C4 grasses. Both the magnitude and timing of this ca. 3.5‰ mean carbon isotopic shift is consistent with data reported previously from numerous late Miocene localities in the northern hemisphere and selected equatorial regions. Analysis of the δ13C values for high-crowned, presumed grazing mammals from post-8 Ma localities between 21 to 35° S lat. (in Argentina and Bolivia) indicate an isotopic gradient in which mean δ13C values (and hence percentage of C3 plants) are proportional to latitude. The δ13C values presented here indicate that the original spread of grasslands during the middle Tertiary, and the so-called "precocious hypsodonty" of corresponding South American herbivores, occurred in a regime of predominantly C3 grasses. The modern ecological landscape in which grasses (and corresponding grassland biomes) are predominantly C4 in mid-latitudes, is a relatively recent global event that is first recorded in South America during the late Miocene and became relatively widespread thereafter.
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The carbon. and oxygen isotope composition of carbonate in enamel hydroxylapatite can provide information on photosynthetic pathways of plants at the base of food webs, and on hydrological conditions. Retrieval of palaeoenvironmental information from isotopic composition of vertebrate fossils is complicated by potential diagenetic overprinting. In this study alteration has been assessed by examining the extent to which expected biological carbon and oxygen isotope patterns are disrupted in fossils of species whose diets cart be independently predicted by other criteria. The biological patterns used are 1) the differences in carbon, isotope composition between grazers and browsers, and 2) the differences in oxygen isotope composition between hippopotamus and terrestrial herbivores. Results obtained on, enamel samples from Tighenif (Algeria, approximate to 700,000 yr), Melka-Kunture (Ethiopia, 0.7-1.5 myr), and Anabo Koma (Djibouti, approximate to 1.6 myr) suggest that in vivo carbon and oxygen isotope compositions are preserved in most cases. Moreover, in all three regions, modern, patterns of C-3 versus C-4 grass dominance were present within the Pleistocene.