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Biological Journal of the Linnean Society, 2014, 112, 657667. With 4 figures

Ecological and life-history correlates of enamel growth

in ruminants (Artiodactyla)
XAVIER JORDANA1*, NEKANE MARN-MORATALLA1, BLANCA MONCUNILL-SOL1
and MEIKE KHLER2,3
1

Institut Catal de Paleontologia Miquel Crusafont (ICP), Universitat Autnoma de Barcelona, 08193
Bellaterra, Barcelona, Spain
2
ICREA at Institut Catal de Paleontologia Miquel Crusafont (ICP), Universitat Autnoma de
Barcelona, 08193 Bellaterra, Barcelona, Spain
3
Departament dEcologia, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, E-08028
Barcelona, Spain
Received 4 November 2013; revised 16 January 2014; accepted for publication 18 January 2014

Enamel incremental markings are widely used to reconstruct growth patterns of extinct mammals. However, the
likely existence of an allometric relationship between dental morphology and enamel growth suggests that caution
is required when making life-history inferences based on these microstructures. In the present study, we aimed to
explore the potential of using enamel growth rate as a reliable proxy of the pace of life in fossil species. We
sectioned 24 permanent first lower molars from 19 extant and two fossil ruminant species. By using polarized light
microscopy, we measured the two parameters that determine enamel growth rates: daily secretion rate (DSR) and
extension rate, as quantified by enamel formation front (EFF) angle. These parameters were regressed against
body mass, hypsodonty index, and relative age at first reproduction (relative to body mass) as a proxy for the
species pace of life, using phylogenetic generalized least squares analyses. Our results indicate that DSR conforms
to the allometric relationship because it is positively correlated with hypsodonty. By contrast, enamel extension
rate is strongly related to the pace of life. These findings suggest that the two mechanisms of enamel growth might
be subject to different selective forces. The application in two fossil species provides evidence that EFF angle is a
reliable proxy of the life history of extinct mammals. 2014 The Linnean Society of London, Biological Journal
of the Linnean Society, 2014, 112, 657667.

ADDITIONAL KEYWORDS: dental growth dental histology diet hypsodonty incremental markings
laminations life cycle mammals paleohistology teeth.

INTRODUCTION
Mammalian teeth are abundant in the fossil record
because they are largely covered by enamel, which
is the best preserved of the hard tissues (Hillson,
2005). The internal microstructure of enamel shows
regular incremental markings as a result of circadian
fluctuations in the rate of matrix production by
ameloblasts (enamel-forming cells) (Dean, 1987, 2006;
Bromage, 1991; Smith & Tafforeau, 2008). These
daily incremental lines in enamel, referred to as

*Corresponding author. E-mail: xavier.jordana@icp.cat

cross-striations and laminations (two structurally

different markings; Kierdorf et al., 2013), allow
determinination of the timing and rates of enamel
formation (Boyde, 1989; Smith, 2006; Kierdorf et al.,
2013).
Because dental development is strongly integrated
into somatic growth and life cycles in mammals
(Smith, 1989, 1991, 2000; Dean, 2006; Kelley &
Schwartz, 2012; Jordana et al., 2013), enamel incremental markings are frequently used as a tool to
reconstruct the life history of extinct species
(Bromage & Dean, 1985; Dean et al., 2001; Schwartz
et al., 2002, 2005; Smith, Martin & Leakey, 2003;
Dirks et al., 2009). However, dental structure and

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X. JORDANA ET AL.

morphology are tightly linked to dietary behaviours

(Hillson, 2005; Famoso, Feranec & Davis, 2013).
Therefore, relative differences in enamel thickness
and/or crown height reflecting dietary adaptations
may lead to differences in enamel growth that are
unrelated to the pace of life. Teeth with relatively
thick/high enamel may result from a longer period of
enamel formation and/or higher rates of enamel
growth (Smith et al., 2003). Thereby, the likely existence of an allometric relationship between dental
morphology and enamel growth suggests that caution
is required in making life-history inferences in fossil
mammal based on enamel incremental markings
(Tafforeau et al., 2007; Dirks et al., 2009; Dirks,
Bromage & Agenbroad, 2011; Jordana & Khler,
2011).
In the present study, we aimed to explore the potential to use enamel growth rates as a reliable proxy of
the pace of life in fossil species. Enamel growth is
essentially determined by two mechanisms (Reid
et al., 1998; Hogg & Walker, 2011: (1) the amount of
enamel secreted by ameloblasts or enamel secretion
rate and (2) the rate at which ameloblasts differentiate along the inner enamel epithelium or enamel
extension rate. The correlates of both parameters with
life-history traits, as well as other factors, such as
enamel thickness, body mass or diet, have been
analyzed in only a few studies on primates (Smith
et al., 2003; Hogg & Walker, 2011). In the present
study, we used ruminants as a mammalian case study.
Ruminants comprise an excellent group for exploring
the correlates of enamel growth rates because they
dwell in different habitats and also display a wide
range of body masses and very different degrees of
crown height (hypsodonty).

MATERIAL AND METHODS

For the present study, we used a sample of 24 permanent first lower molars from 19 extant and two
fossil ruminant species (Table 1). Teeth were sectioned in accordance with standard procedures in our
laboratory (Jordana & Khler, 2011). The molars were
embedded in epoxy resin (Araldite 2020) and sectioned through the mesial cusps in the bucco-lingual
plane using a Buehler Isomet diamond low speed saw.
The surface of interest of the tooth block was polished
with carborundum powder of decreasing particle size
and bonded to a glass slide using ultraviolet curing
glue (Loctite 358). Each specimen was sectioned and
ground to a thickness of approximately 130 m using
a diamond saw (PetroThin; Buehler). The final thickness was obtained by hand polishing with a gradient
of carborundum until roughly or around 90 m.
Finally, the thin section was mounted with a DPX

medium (Scharlau) that preserves and enhances the

visualization of the microstructure.
Polarized light microscopy (Zeiss Scope.A1 with
digital camera AxioCam ICc5) and image analysis
software (IMAGEJ) were used to calculate the parameters of enamel growth. Laminations, comprising
regular lines that follow the course of the developing
enamel front, appear to be the most common incremental markings in the enamel of ungulate species
(Tafforeau et al., 2007; Jordana & Khler, 2011;
Kierdorf et al., 2012, 2013). There is empirical evidence of their daily nature (Iinuma et al., 2004;
Kierdorf et al., 2013), similar to the prism crossstriations in primate enamel (Smith, 2006). Therefore,
the amount of enamel secreted by the ameloblast per
day (daily secretion rate; DSR) was quantified measuring the distance between adjacent laminations along
the course of the prism (Jordana & Khler, 2011). The
enamel extension rate or the rate at which new secretory ameloblasts differentiate along the enamel formation front (EFF) was quantified by measuring the
enamel formation front angles (EFF angles), as represented by the lamination and the enameldentine
junction (EDJ) (Boyde, 1964; Shellis, 1984; Hogg &
Walker, 2011). Therefore, smaller EFF angles represent a faster extension rate because a larger number of
cells is activated along the inner enamel epithelium to
secrete enamel in a given time (Smith et al., 2003)
Previous studies have shown that enamel growth
rate vary considerably from early to later stages
of molar crown formation (Jordana & Khler, 2011;
Kierdorf et al., 2013). The parameters of enamel
growth (DSR and EFF angle) should be measured at
equivalent zones and regions to allow comparisons. To
standardize, a measurement protocol was employed.
Because the analyzed teeth showed different degrees
of occlusal wear, in the present study, enamel growth
parameters were measured just at the cervical third
of the crown, taking into account the estimated total
height of the unworn crown. Specifically, the parameters were measured in 20 micrographs of successive
regions along the linguolateral enamel of the mesial
cusp (Fig. 1). In each micrograph, wherever laminations were discernible in the central enamel, the
distance along the prism course between several
successive laminations was measured and the value
was divided by the number of daily markings that
it crosses, giving the DSR. Furthermore, discernible
EFF angles were measured in the micrograph and
then the values were averaged. The DSR and EFF
angle for each specimen were obtained by averaging
the values in each micrograph or region. For the few
species including two samples (Table 1), the species
mean was calculated.
The enamel growth parameters (DSR and EFF
angle) from each species were regressed against body

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LIFE-HISTORY CORRELATES OF ENAMEL GROWTH

659

Table 1. Sample used in the present study

Section

Collection

Subfamilies

Species

Sex

Site

Institution

IPS69510

S2971

Bovinae

Zoolog. Garden Hannover

ZIHU

IPS74166

S6875

Bovinae

Zoolog. Garden Berlin

ZIHU

IPS56201

S7719

Bovinae

South Africa, Umfolozi

ZIHU

IPS56205

S5645

Bovinae

Angola, Tumba Grande

ZIHU

IPS56207
IPS56208
IPS7006

S7735
S7722
IPS7006

Bovinae

Angola, Culele/Camata

ZIHU

Spain, Torrent de Traginers

ICP

IPS56217
IPS56218
IPS74162

S5671
S5672
S5463

M, F

Angola, Capolopopo

ZIHU

Antilopinae

unknown

ZIHU

IPS56228

S7987

Antilopinae

Chad, Abch

ZIHU

IPS56230

S7988

Antilopinae

Tanzania, Lolkisale

ZIHU

IPS56234

S7536

Antilopinae

Zoolog. Garden Hannover

ZIHU

IPS56226

S5691

Antilopinae

Angola, Capolopopo

ZIHU

IPS56247

S6414

Cephalophinae

Zoolog. Garden Frankfurt

ZIHU

IPS56215

S5684

Aepycerotinae

Angola, Ruacan

ZIHU

IPS74165

S5926

Caprinae

unknown

ZIHU

MBCN15799

Caprinae

Spain, Cova Moleta

MBCN

IPS74173

S5668

Alcelaphinae

Angola, Cuangar/Cubango

ZIHU

IPS74168

S7830

Hippotraginae

Chad, Ouadi Achim

ZIHU

IPS60870
IPS56303
IPS82014

IPS60870
IPS56303
S4633

Cervinae

Spain, Badajoz/Austria,
Viena
Zoolog. Garden Hannover

ICP

Capreolinae

ZIHU

IPS73888

IPS73888

Capreolinae

Boselaphus
tragocamelus
Bubalus
depressicornis
Tragelaphus
angasii
Tragelaphus
scriptus
Tragelaphus
spekii
Tragoportax
gaudryi *
Oreotrgaus
oreotragus
Saiga
tatarica
Eudorcas
rufifrons
Eudorcas
thomsonii
Gazella
dorcas
Antidorcas
marsupialis
Cephalophus
zebra
Aepycerus
melampus
Hemitragus
jemlahicus
Myotragus
balearicus *
Connochaetes
taurinus
Oryx
dammah
Cervus
elpahus
Rangifer
tarandus
Capreolus
capreolus

Spain, Lleida

ICP

Bovinae
Antilopinae

*Fossil species. ZIHU, Zoological Institute of Hamburg University; ICP, Institut Catal de Paleontologia Miquel
Crusafont; MBCN, Museu Balear de Cincies Naturals. M, male. F, female. ?, unknown.

mass (BM), hypsodonty index (HI) and relative age at

first reproduction (AFRres). The body mass of some
wild specimens was known (see Khler, Moy-Sol &
Esteban-Trivigno, 2008). The sex-specific mean adult
body mass for the other species comes from the literature (Table 2). Hypsodonty index (of the m3) of
extant species come from Janis (1988) and Mendoza

& Palmqvist (2008). Data of the average age at first

reproduction of living species, taking into account
the sex, were obtained from the literature (Table 2).
BM and HI of fossil Myotragus balearicus were
obtained from Jordana et al. (2012). BM of fossil
Tragoportax gaudryi was obtained from Moy-Sol
(1983). HI of fossil T. gaudryi was measured sensu

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X. JORDANA ET AL.

Figure 1. A, longitudinal section through the mesial cusps of the Antidorcas marsupialis first lower molar (IPS56226)
observed under cross-polarized light. Scale bar = 1000 m. B, detail of the linguolateral enamel of the paraconid shown
in (A) (frame). White lines indicate the successive daily incremental markings referred to as laminations. Dashed arrow
indicates the prism direction. Dashed line indicates the enamel-forming front. EDJ, enameldentine junction. Scale
bar = 100 m.

Janis (1988). AFR of both fossil species was estimated

by bone histology (Khler & Moy-Sol, 2009;
Marn-Moratalla et al., 2012).
Age at first reproduction provides reliable information about the position of a given species on
the slowfast life-history continuum (Gaillard et al.,
2000). In the present study, however, we used AFRres
as a proxy for the species pace of life to correct the
scaling effect on the life-history traits when species
of different body size are compared (Stearns, 1992;
Calder, 1996). We calculated the residuals of AFR
(AFRres) when this parameter is regressed against
body mass (as an independent variable), with both
variables log-transformed (Marn-Moratalla et al.,
2014). This means that species with higher values of
AFRres grow more slowly (i.e. slower life history).
We
conducted
multiple
regressions
using
phylogenetic generalized least squares analyses
(pglmEstLambda in R package; CAIC library), with
BM, HI, and AFRres as predictor variables, and with
DSR and EFF angle as dependent variables. PGLS
analysis computes the least squares regression
taking into account the extent of phylogenetic non-

independence (Harvey & Pagel, 1991; Orme et al.,

2009). The synthetic phylogenetic tree with the
species used in the PGLS analyses is illustrated
in Figure 2. This tree is based on a phylogenetic
supertree that includes all 197 extant and recently
extinct species of the suborder Ruminantia
(Hernndez-Fernndez & Vrba 2005).
In the present study, we also calculated enamel
growth parameters for two fossil ruminant species:
the insular dwarf bovid M. balearicus Bate, 1909 and
the continental bovid T. gaudryi Moy-Sol, 1983.
Our fossil species were not included in the PGLS
analyses. They were only used to test to what extent
the results of this study apply to fossils.

RESULTS
The mean DSR and EFF angle in the species of our
ruminant sample are shown in Table 2. In the extant
sample, DSR values range from 8.9 m day1 in the
zebra duiker (Cephalophus zebra) to 17.3 m day1 in
the blue wildebeest (Connochaetes taurinus). EFF

2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 657667

Tragoportax gaudryi
Myotragus balearicus

Boselaphus tragocamelus
Bubalus depressicornis
Tragelaphus angasii
Tragelaphus scriptus
Tragelaphus spekii
Oreotrgaus oreotragus
Saiga tatarica
Eudorcas rufifrons
Eudorcas thomsonii
Gazella dorcas
Antidorcas marsupialis
Cephalophus zebra
Aepycerus melampus
Hemitragus jemlahicus
Connochaetes taurinus
Oryx dammah
Cervus elpahus
Rangifer tarandus
Capreolus capreolus
10
9

7
8
14
4
9
17
5
5
9
6
6
8
7
6
4
3
9
5
4

13.40 1.23
9.87 1.04

14.12 1.75
12.99 2.11
11.78 3.15
13.28 1.44
10.76 1.74
11.57 1.05
15.05 1.04
12.62 0.44
14.13 1.49
13.28 1.23
15.80 0.72
8.99 1.98
15.16 1.06
11.58 0.40
17.31 0.68
13.75 3.11
12.95 2.01
14.17 0,81
12.24 1.81

Mean SD

6
5

5
5
6
5
10
9
5
6
7
5
5
5
6
5
3
3
12
6
7

5.11 0.74
11.62 1.59

4.33 2.38
4.26 1.59
5.71 1.60
5.78 2.09
5.77 2.31
5.27 2.76
4.10 1.04
4.22 1.19
4.16 1.53
5.68 1.12
3.14 1.57
5.65 0.83
6.41 1.10
5.73 2.98
3.48 3.15
5.36 0.91
5.53 1.19
5.93 1.41
5.01 1.66

Mean SD

EFF angle

2.0
6.1

3.0
4.4
2.5
2.5
2.9
3.8
5.3
3.8
3.8
3.6
4.9
1.2
4.9
5.0
4.9
3.4
2.1
1.5
1.5

HI

55.0
26.0

200.0
250.0
135.0*
32.0*
73.0*
14.0*
35.0
25.0*
21.0*
17.5
36.0*
17.5
60.0*
55.0
227.5*
135.0*
170.0
109.1
30.0

BM (kg)

2.0
8.0

3.5
2.5
3.5
3.5
4.0
1.5
2.0
2.0
1.0
2.0
1.0
2.0
4.0
4.0
4.5
3.0
5.0
3.0
3.0

AFR
(years)

0.14
0.55

0.05
0.23
0.00
0.20
0.15
0.05
0.05
0.01
0.28
0.04
0.36
0.04
0.17
0.19
0.04
0.06
0.13
0.03
0.15

AFRres

DSR, daily secretion rate (m day1); EFF angle, enamel-forming front angle (degrees); N, number of micrographs for which measurements were taken; HI,
hypsodonty index; BM, body mass; AFR, age at first reproduction; AFRres, relative age at first reproduction.
*Data of the specimen.
Data for the species sensu Clutton-Brock, Guinness & Albon (1982), Moy-Sol (1983), Estes (1991), Yom-Tov, Mendelssohn & Groves (1995), Kingdon (1997),
Nowak (1999), Cain, Krausman & Germaine (2004), Kate et al. (2009), Khler & Moy-Sol (2009), Gaspar-Lpez et al. (2010), Marn-Moratalla et al. (2012),
Jordana et al. (2012).
Residuals of AFR using just the living species.
Residuals of AFR using all species.

Fossil taxa
Bovinae
Caprinae

Cephalophinae
Aepycerotinae
Caprinae
Alcelaphinae
Hippotraginae
Cervinae
Capreolinae

Antilopinae

Living species
Bovinae

Species

DSR

Table 2. Data included in the analyses in the present study

LIFE-HISTORY CORRELATES OF ENAMEL GROWTH

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X. JORDANA ET AL.

Figure 2. Phylogenetic tree with the species used in

the phylogenetic generalized least squares analyses in the
present study. Based on a supertree of the suborder
Ruminantia compiled by Hernndez-Fernndez & Vrba
(2005).
Table 3. Results of the phylogenetic generalized least
squares analyses
Dependent (y)

Predictors (x)

EFF angle

Adjusted r2

0.48

0.004
0.004
0.129
0.453
0.039
0.493
0.027
0.198

AFRres
HI
BM
DSR

0.29
AFRres
HI
BM

DSR, daily secretion rate; EFF angle, enamel-forming

front angle; HI, hypsodonty index; BM, body mass;
AFRres, relative age at first reproduction. P < 0.05 was
considered statistically significant.

angles range between 3.1 in the springbok

(Antidorcas marsupialis) and 6.4 in the impala
(Aepycerus melampus).
Results from PGLS analyses are shown in Table 3.
EFF angle correlates significantly with the AFRres,
whereas DSR correlates significantly with HI. The
former correlation is more reliable than the latter
(Fig. 3, Table 3). The other predictors were not statistically significant. Importantly, body mass does not
correlate with DSR, nor with EFF angle.
Regarding fossil species, the insular bovid M.
balearicus shows a very high EFF angle value (11.6)
that fits with its outstanding AFRres value. However, it shows a low DSR (9.8 m day1) relative to

Figure 3. Scatter plots including extant and fossil ruminants. Regression lines calculated just with the living
species. A, enamel formation front (EFF) angle against relative age at first reproduction (AFRres), r2 = 0.48. B, daily
secretion rate (DSR) against hypsodonty index (HI), r2 =
0.31. Tg, Tragoportax gaudryi; Mb, Myotragus balearicus.

its exceptional HI. The continental fossil bovid

T. gaudryi displays an intermediate EFF angle value
(5.1) that fits well with its AFRres value. This
fossil bovid shows a DSR of 13.4 m day1, which is

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663

Figure 4. Micrographs showing enamel formation front (EFF) angles [the angle between EFF and enameldentine
junction (EDJ)] in equivalent regions of the fossil species. The small white lines indicate successive laminations. Scale
bar = 50 m. A, Tragoportax gaudryi IPS7006. B, Myotragus balearicus MBCN15799.

moderately high relative to its low HI but within the

range of variation of our extant sample (Figs 3, 4).

DISCUSSION
An allometric relationship between the degree of
hypsodonty and enamel growth rate in ruminants
might bias inferences from enamel incremental markings about the pace of life of fossil species.
Our results from an extant ruminant sample
indicate that the daily secretion rate per ameloblast
(DSR) shows a positive allometric relationship with
the HI (Fig. 3B). However, this relationship is not so
reliable and hence a larger sample would be required
to support this evidence. Our measures of DSRs in
ruminants range between 9 and 17 m day1 and correspond well with previous experimental findings in
other ruminants using vital labellings (Iinuma et al.,
2004; Kierdorf et al., 2013). In primates, DSRs are
considerably lower, ranging approximately between 2
and 7 m day1 (Smith et al., 2003; Smith, 2008; Hogg
& Walker, 2011). The high secretory activity of the
ameloblasts in artiodactyls is most likely related to
the relatively higher crowns of their molars.
By contrast, the enamel extension rate, as quantified by EFF angle, is strongly related to the AFRres,
and thus to the species pace of life. Therefore, in our
sample, the slowly growing species (higher AFRres
values; Fig. 3A, Table 2) tend to exhibit wider angles
(higher EFF angle values) between the enamel incremental markings (laminations) and the EDJ than
faster growing species. This indicates that, in species
with a slower life history, a smaller number of

ameloblasts is activated along the inner enamel epithelium to secrete enamel in a given time than in
fast-growing species. The obvious reason for their
slower enamel extension rates is that they have relatively more time to grow the teeth. In mammals,
molar development and eruption are highly adapted
to the rate of post-natal somatic growth (Smith,
2000). Our findings suggest that the amount of
enamel-forming cells that differentiate along the EDJ
in a given time is the mechanism of enamel growth
more closely linked to somatic growth than the
amount of enamel secreted by the ameloblasts.
In a previous study, Hogg & Walker (2011) already
found that higher values of EFF angle were related to
slower life histories (lengthened juvenile period and
lower birth rates) in Cebidae (Primates). Our study
shows that this can also be applied to ruminants. In
Cebidae (Hogg & Walker, 2011), the species means of
EFF angles range between 9 and 36, whereas, in our
extant ruminant sample, EFF angles range from 3 to
6. The highest rates of enamel extension in ruminants probably not only reflect their larger teeth, but
also their faster life histories. However, we can not
exclude that the phylogeny and/or dental morphology
and function have an impact on the rate of enamel
extension when comparing very different groups of
mammals (i.e. primates and artiodactyls). Therefore,
we consider that these values are not directly comparable across different groups of mammals when
classifying species along the slowfast life-history
continuum.
Importantly, in the present study, body mass BM
does not correlate significantly with DSR, nor with

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X. JORDANA ET AL.

EFF angle, which is in agreement with the study on

Cebids (Hogg & Walker, 2011). Bromage et al. (2002)
and Dirks et al. (2011) found similar DSR values
in large (Mammuthus columbi and Elephas recki,
> 7000 kg) and dwarf (Palaeoloxodon cypriotes,
200 kg) fossil elephantid taxa. At odds with our findings in ruminants, however, they suggested that
extension rates are the primary mechanism in creating teeth with different crown heights in elephantids
(Dirks et al., 2011). Nevertheless, we must note that
they were talking about absolute height and not relative height (HI).
We are aware of our small sample size and of the
significant limitation of using almost only a single
specimen per species. Furthermore, we must also take
into account that some specimens originate from zoos.
However, we consider our sample as representative of
ruminant diversity (nine subfamilies are represented).
Moreover, we found a great similarity between the
values of the enamel growth parameters for the few
species including two samples. This result was not
unexpected because, in mammals, tooth development
is tightly integrated in their life cycles, and so it is a
very conservative trait (Smith, 1989, 1991, 2000). We
can state, therefore, that these results provide preliminary evidence of the relationship between enamel
extension rate and the pace of life in ruminants.

APPLICATION

On the other hand, M. balearicus displays a

low value of DSR, although within the variations
observed in extant ruminants, which contrasts with
its high hypsodonty (Fig. 3B). This suggests that the
extreme pressure to reduce growth rate, and enhance
fitness in a resource-limited environment, essentially
resulted in a slower extension rate and, to a lesser
extent, in a lower enamel secretion rate. Indeed,
Jordana et al. (2012) suggested that the outstanding
hypsodonty in M. balearicus was the outcome not
only of high rates of tooth wear, but also of selection
for increased durability of the permanent dentition
in association with an extended lifespan (slower life
history).
Tragoportax gaudryi (Bovidae, Bovinae) is a Late
Miocene bovid from Western Europe belonging to the
tribe Boselaphini (Moy-Sol, 1983). The life-history
strategy of this fossil species, as inferred from bone
histology (Marn-Moratalla et al., 2012), is similar to
that of its relative Buselpahus tragocamelus and
faster than that of extant Tragelaphini (a sister
clade of Boselaphini) of similar body size, such as
Tragelaphus scriptus or Tragelaphus spekii (Table 2).
The EFF angle value calculated for T. gaudryi in
the present study fits well with the above findings.
Moreover, the daily enamel secretion rate (DSR) is
within the range of variation of mesodont ruminants
(as T. gaudryi) of our sample (Fig. 3).

TO FOSSIL SPECIES

Myotragus balearicus (Bovidae, Caprinae) is the terminal species of an endemic genus from Balearic
Islands that survived under complete geographical
isolation for over 5 Myr, from Pliocene to mid Holocene
(Alcover, Moy-Sol & Pons-Moy, 1981). Previous
work indicated an exceptional slow pace of dental
development in this fossil bovid that was coupled
with an exceptionally slow somatic growth rate
and a delayed age at reproductive maturity (Khler
& Moy-Sol, 2009; Jordana & Khler, 2011;
Marn-Moratalla et al., 2011; Jordana et al., 2013).
This evolution towards a slow life history has been
suggested to result from changes in energy allocation
from reproduction to growth and maintenance that
facilitated survival in a resource-limited environment
without predators (Khler, 2010; Jordana et al., 2012).
In the present study, we found very wider angles
between laminations and EDJ (very high values of
EFF angle; Fig. 4B) in M. balearicus that lie outside
the variations observed in living ruminants and
approach the values of primates. This result is in
agreement with the above findings and fits well with
an exceptional age at maturity of approximately 8
years (relative to its body size of 26 kg) estimated
based on bone histology (Khler & Moy-Sol, 2009;
Marn-Moratalla et al., 2011) (Fig. 3A).

CONCLUSIONS
The results of the present study on extant ruminants
suggest that the enamel secretion rate by ameloblast
correlates positively with the HI. On the other hand,
the enamel extension rate is strongly related to the
pace of life; that is, at a given time, a smaller number
of enamel-forming cells (ameloblasts) are activated
along the inner enamel epithelium in slowly growing
species than in fast-growing ones.
Our findings suggest that the two mechanisms
determining enamel growth rates, secretion and
extension, are subject to different selective forces. On
the one hand, enamel secretion rates appear to
be more influenced by the ecological pressures (diet)
that determine tooth morphology. On the other hand,
enamel extension rates are tightly related to the
species life history, and hence shaped by the same
ecological factors (extrinsic mortality and resource
availability).
The application of these results to two fossil species
provides evidence that the quantification of enamel
formation front angles (EFF angle), as represented by
the lamination and the EDJ, is a reliable proxy of the
ranking of fossil mammals along the slow-fast life
history continuum within phylogenetically related
groups.

2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 657667

LIFE-HISTORY CORRELATES OF ENAMEL GROWTH

ACKNOWLEDGEMENTS
We thank all of the individuals and institutions that
provided us with the extant sample of ruminants: Th.
Kaiser for permission to cut teeth of skeletons from
the collections of the Zoological Institute of Hamburg
University; W. Arnold (Research Institute of Wildlife
Ecology, Wien) for providing alpine red deer material;
and Asociacin del Corzo Espaol (G. Pajares and
E. Melero), J. A. Ruiz (Gobierno de la Rioja), and
I. Snchez for roe deer and red deer skeletons
from Iberian Peninsula. We also are grateful to
C. Constantino for access to the collections of
M. balearicus at the Museu Balear de Cincies Naturals (Sller, Mallorca). We thank three anonymous
reviewers for their helpful comments. Many thanks
are extended to A. Houssaye for her invitation to
present this manuscript in the special issue New
Advances in Paleohistological Studies as well as Prof
John A. Allen (Editor of Biological Journal of the
Linnean Society). This work was supported by the
Spanish Ministry of Economy and Competitiveness:
CGL2012-34459 (PI: MK). XJ is supported by a Juan
de la Cierva postdoctoral grant from the Spanish
Ministry of Economy and Competitiveness (reference
JCI-2010-08157). NMM is supported by a FPI Grant
from the Spanish Ministry of Economy and Competitiveness (reference BES-2009-02641). BMS is supported by a FPU grant from the Spanish Ministry of
Education (reference AP2010-2393).

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