Structure and evolution of mammoth molar enamel
MARCO P. FERRETTI
Ferretti, M.P. 2003. Structure and evolution of mammoth molar enamel. Acta Palaeontologica Polonica 48 (3): 383–396.
This work investigates the structure of Eurasian Plio–Pleistocene Mammuthus enamel, with attention to diagenesis and
individual variability. A focal point of this study was to determine whether morphological trends in Mammuthus molars
were accompanied by correlated enamel microstructure changes. In the examined four taxa the enamel of the cheek teeth
consists of three layers delimited by two major discontinuities in enamel prism direction. Noticeably, the enamel capping
the occlusal end of the unworn molar plates retains a less derived two−layered structure, similar to that found in the basal
proboscidean Moeritherium.InMammuthus meridionalis the third deciduous premolar is differentiated from all other
teeth in having more strongly decussating Hunter−Schreger bands in the middle layer, as a possible reinforcement of the
very thin enamel. Evidence from this analysis shows that, in the transition from late Middle Pliocene M. rumanus to Late
Pleistocene M. primigenius, the middle enamel layer, which is made up of prisms at an angle to the occlusal surface, pro−
viding greater resistance against wear, increased its relative thickness. This is consistent with the hypothesis that
Mammuthus adapted to a more abrasive diet. Comparison with other proboscidean taxa indicates that the schmelzmuster
(enamel pattern) found in Mammuthus is a synapomorphy of the Elephantoidea.
Key words: Mammalia, Proboscidea, Mammuthus, enamel microstructure, evolution, systematics.
Marco P. Ferretti [firstname.lastname@example.org], Dipartimento di Scienze della Terra and Museo di Storia Naturale, Sezione di
Geologia e Paleontologia, University of Firenze, via G. La Pira 4, I−50121 Firenze, Italy.
Enamel microanatomy has become an important feature in the
taxonomy and phylogeny of several mammal groups
(Korvenkontio 1934; Kawai 1955; Boyde 1965, 1969, 1971;
Koenigswald 1980; Carlson and Krause 1982; Gantt 1983;
Sahni 1985; Koenigswald et al. 1993; Martin 1993, 1994;
Pfretzschner 1993; Koenigswald and Sander 1997a; Stefen
1997; Kalthoff 2000). Enamel mechanical properties, espe−
cially resistance to wear and fracture propagation, were also
demonstrated in recent studies (Rensberger and Koenigswald
1980; Fortelius 1985; Pfretzschner 1988, 1994; Rensberger
1992, 1995a, b, 1997; Srivastava et al. 1999), providing an im−
portant complement to morpho−functional analysis of teeth for
interpreting the feeding habits of fossil vertebrates.
Proboscidean enamel has been the subject of several stud−
ies that have highlighted the group’s complex enamel struc−
ture and discussed some functional adaptations (Remy 1976;
Kozawa 1978, 1985; Okuda et al. 1984; Bertrand 1987,
1988; Sakae et al. 1991; Pfretzschner 1992, 1994; Kamiya
1993; Ferretti 2003).
Previous studies found five principal enamel types occur−
ring in the various proboscidean families (Kozawa 1978;
Bertrand 1987, 1988; Pfretzschner 1994). Four of them are
common among placental mammals (Koenigswald 1997).
A fifth, very complex enamel type, is restricted to the Pro−
The present paper is a contribution to knowledge of
enamel microstructure of mammoths. Four mammoth spe−
cies of the Eurasian Mammuthus lineage were investigated,
focusing on individual variability of the structure of the mo−
lar enamel, with attention to possible alteration due to
Mammuthus is a monophyletic genus; with respect to
Elephas and Loxodonta, it is distinguished on both morpho−
logical and molecular evidence (Maglio 1973; Shoshani et al.
1985; Tassy and Darlu 1986; Lister 1996; Thomas et al.
2000). The three elephant genera Loxodonta,Elephas, and
Mammuthus diverged as early as the Early Pliocene, around
5 Ma, or somewhat earlier (Maglio 1973; Beden 1987; Kalb
and Mebrate 1993). Thus Mammuthus dispersed outside of
Africa to Eurasia in the Middle Pliocene. The last Mammu−
thus representative, the woolly mammoth M. primigenius
(Blumenbach, 1799), became extinct about 3.7 thousand
years ago (Lister and Bahn 2000). During the approximately
3 million years covered by the four Mammuthus species ex−
amined here, mammoth molars underwent a morphological
change characterized by increment of crown height, multipli−
cation of the number of plates forming the tooth, and thin−
ning of the enamel, as a probable adaptation to a progres−
sively predominant grass diet. These modifications could
have also affected enamel microstructure and its verification
is one of the aims of this paper.
Terminology and abbreviations
For description of enamel microstructure the terminology of
Carlson (1995), and Koenigswald and Sander (1997) was
Acta Palaeontol. Pol. 48 (3): 383–396, 2003
Enamel microstructure terminology and abbreviations.—
Enamel cement junction (ECJ): the boundary plane between
enamel and crown cement; enamel dentine junction (EDJ):
the boundary plane between dentine and enamel. During
tooth formation, amelogenesis starts at the EDJ; enamel
prism: bundles of apatite cristallites extended from the EDJ
close to the outer enamel surface; Hunter−Schreger bands
(HSB): a specific mode of prism decussation, with prisms de−
cussating in layers. Prisms within one HS band are oriented
parallel to one another, and at an angle to prisms in adjacent
bands; interprismatic matrix (IPM): the apatite cristallites be−
tween prisms; outer enamel surface (OES): the outer limit of
enamel (in elephant molars, the OES is usually covered by
cement); prism decussation: crossing over of prisms or
groups of prisms, due to lateral bending of prisms along their
way from the EDJ to the OES; prism sheath: boundary plane
produced by an abrupt change in apatite cristallite orien−
tation, delimiting a single enamel prism.
Abbreviations of collections and institutions.—KOE, enamel
collection of the Institut für Paläontologie, Rheinische Frid−
rich−Wilhelms−Universität Bonn, Germany; IGF, Museo di
Storia Naturale – Sezione di Paleontologia e Geologia,
Universitàdegli Studi di Firenze, Italy; IQW, Forschungs−
institut und Naturmuseum Senckenberg Forschungsstation
für Quartärpalaeontologie, Weimar, Germany; MAA,
Museo Archeologico, Arezzo, Italy.
Other abbreviations.—M, upper molar; m, lower molar; DP,
deciduous upper premolar; dp, deciduous lower premolar.
Material and methods
Fossil teeth of Mammuthus meridionalis (Nesti, 1825) from
Upper Valdarno (Italy; early Early Pleistocene; Azzaroli
1977) were sectioned for enamel microstructure analysis un−
der the SEM and the light microscope. Five of the six cheek
teeth constituting mammoth primary and adult dentition,
were sampled. These teeth are here referred to as deciduous
third (DP3) and fourth (DP4) premolar; first (M1), second
(M2), and third (M3) molar (lower case characters are used
for corresponding lower teeth). Further comparative material
was prepared and examined in order to cover the successive
Plio–Pleistocene Eurasian mammoth species and the two ex−
tant elephant species (Table 1). The comparative material in−
cludes specimens of: M. rumanus (Stefanescu, 1924), from
Montopoli (Italy; late Middle Pliocene), representing the ear−
liest occurrence of Mammuthus in Western Europe, (Azza−
roli 1977; Lister and Sher, 2001; Lister and van Essen 2003);
M. meridionalis from Pietrafitta and Farneta (Italy; late Early
Pleistocene; Ferretti 1999); M. trogontherii (Pohlig, 1885)
from Süssenborn (Germany; early Middle Pleistocene;
Günther 1969); M. primigenius from various European late
Middle Pleistocene to Late Pleistocene localities; Elephas
maximus Linnaeus, 1758 (Recent); Loxodonta africana
(Blumenbach, 1797) (Recent). The four Mammuthus taxa in−
vestigated in this work are morphologically coherent units
with a defined boundary in time and space (Fig. 1), distin−
384 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
Table 1. List of specimens analyzed in this study.
Taxon Specimen Locality Age
Mammuthus rumanus IGF 19321, M3 Montopoli, Italy late Middle Pliocene
Mammuthus meridionalis IGF 12787, M1 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 13730a, M2 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 44, M2 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 13730b, M3 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 1147, M3 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 145, dp3 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 151, dp4 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF 69, m3 Upper Valdarno, Italy Early Pleistocene
Mammuthus meridionalis IGF P−61, M3 Farneta, Italy late Early Pleistocene
Mammuthus meridionalis IGF−PM1, m3 Pietrafitta, Italy late Early Pleistocene
Mammuthus trogontherii IQW 3046, M3 Süssenborn, Germany early Middle Pleistocene
Mammuthus primigenius IGF 1086b, M3 Arezzo, Italy late Middle Pleistocene
Mammuthus primigenius KOE 389 M3 Sickenhofen, Germany Late Pleistocene
Mammuthus primigenius IGF 2289, m1 Tiber Valley, Italy Late Pleistocene
Elephas maximus IGF−E1, m3 India Recent
Loxodonta africana KOE 164, M? zoo specimen Recent
Loxodonta africana IGF−L1, M2 zoo specimen Recent
1Specimen previously attributed to Archidiskodon gromovi (Aleskeeva and Garutt, 1965) by Azzaroli (1977).
guished from each other by morphological differences that
are quite stable across fossil samples (Lister 1996; Lister and
Sher 2001). Current evidence makes it increasingly likely
that they are not just successive samples from a reproductive
continuum (i.e., chrono−species), but, actually, that each
younger taxon is the product of a cladogenetic event
(allopatric speciation) of its corresponding ancestral species
(Lister and Sher 2001; Ferretti 1999). This is here interpreted
as evidence in support of their status as “real” species.
From each molar or molar fragment, small portions of dental
tissue were removed and their position with respect to the
complete tooth recorded. Enamel samples were then embed−
ded in epoxy resin and sawn according to defined planes of
sections (see below) with a circular diamond saw for miner−
alogical sampling. Sections were polished with wet alumi−
num oxide powder from coarser to finer (grit number 400,
600, and 1000) and then etched with 2N HCl for 2–5 sec−
onds, in order to render visible prisms. After this step speci−
mens underwent different preparation according to the
method of analysis (see below). Occlusal enamel fragments
were examined without preparation.
Thin sections.—Polished enamel surfaces were glued on
slides using a transparent two−component epoxy glue. Speci−
mens were then ground to a thickness of about 10 micro−
metres, followed by polishing and etching with HCl 2N for
2–3 seconds. Finally, thin sections were covered with a
coverslip fixed with a photo−hardening glue.
SEM.—Samples for SEM analysis were glued on aluminum
stubs using a conductive carbon paint and then coated with
gold−palladium alloy or with graphite. The latter was used to
prepare specimens for microprobe microanalysis.
Reflected light microscopy.—Coated enamel sections were
examined under the reflected light microscope using the op−
tic−fiber effect of prisms (Koenigswald and Pfretzschner
1987). This method allowed a rapid documentation of rela−
tively large enamel portions.
Planes of section
In order to achieve a three−dimensional reconstruction of the
enamel structure, sections of enamel were examined in vari−
ous planes. Plane orientation is relative to the tooth vertical
axis (occlusal−basal axis; Fig. 2), to the EDJ or to the OES.
For thin sections sagittal (parallel to the tooth occlusal−basal
and mesio−distal axes) and horizontal (perpendicular to the
occlusal−basal axis) planes were prepared. In addition to
these, tangential (parallel to the OES) and oblique (relative to
the EDJ) sections were prepared for SEM and reflected light
Measurement of enamel thickness
In order to quantify differences among taxa in relative thick−
ness of the layers forming the molar enamel (see below),
mean percentage thickness of each layer relative to the whole
enamel thickness, has been calculated. Measurements of
enamel layer thickness were made using a micrometric cur−
sor connected to a light microscope. Measurements were
taken along a line perpendicular to the EDJ. As enamel thick−
ness may vary locally along the enamel section, a minimum
of three measurements was taken at different sites on each
section (sagittal), and a mean value then calculated for each
FERRETTI—STRUCTURE AND EVOLUTION OF MAMMOTH MOLAR ENAMEL 385
Montopoli (ca. 2.6 Ma)
Upper Valdarno (ca. 1.8 Ma)
Farneta; Pietrafitta (ca. 1.4 Ma)
Süssenborn (ca. 600 ka)
Arezzo (ca. 190 ka)
Tiber valley; Sickenhofen
Fig. 1. Chronological distribution of Mammuthus species in Europe and
ages of fossil samples considered in this study.
Fig. 2. Schematic representation of a mammoth lower molar. Anatomical
features, distribution of dental hard−tissues on the occlusal surface, and
principal directions are shown.
specimen. Further measurements were then added and the
mean newly calculated, until the addition of the last measure−
ment did not modify significantly (P < 0.05) the mean from
the previous score.
Enamel types and schmelzmuster
Enamel types are defined on the basis of the direction of the
prisms relative to the EDJ (Koenigswald and Clemens 1992).
Inclination of prisms was measured as the angle between
prism and the normal to the EDJ, according to Korvenkontio
The term schmelzmuster, introduced by Koenigswald
(1980), refers to the spatial distribution of the various enamel
types within a single tooth. The structural organization of
enamel (schmelzmuster) was here considered independently
from the thickness of the various enamel types (differential
The following description summarizes the morphological
characters of the enamel common to all the considered Mam−
muthus meridionalis molars.
Apatite crystallites, the basic constituent of enamel prisms,
are parallel to each other and to the prism long axis. Crystal−
lites in the interprismatic matrix are also oriented parallel to
the neighboring prisms.
Prisms cross section
In their course from the EDJ to the OES, prisms vary both in
cross section and absolute size. The predominant prism type
is the key−hole pattern (type 3 of Boyde 1965). In the inner
enamel prisms are arcade−shaped with a diameter of about
5–6 microns (Fig. 3A1). More outwardly, prisms widen
slightly and develop two lateral expansion (lobes) producing
the so called “ginko−leaf” morphology (Kozawa 1978), typi−
cal of proboscidean enamel (Fig. 3A2). In the outer enamel,
prisms more markedly augment their diameter, while their
cross section becomes more simple, losing the ginko−leaf
outline (Fig. 3A3, C). Frequent in this zone is the apparent fu−
sion between contiguous prisms. This unique feature would
have important implications for the understanding of enamel
formation. However, the possibility that either diagenesis
(but see below) or the sample preparation technique could
have caused the disappearance of part of the (originally pres−
ent) prism sheath, cannot be ignored. Ongoing analyses are
specifically addressing this point.
Restricted to a very thin zone near the OES, a basically
different prism type is found, characterized by small, sub−
circular and irregularly spaced prisms, separated by abun−
dant interprismatic matrix (IPM). Prism sheaths are open ba−
sally or, in some places, they completely surround the prisms
2), a pattern that can be considered intermediate
between type 1 and 3 of Boyde (1965).
3−D enamel.—The three−dimensional pattern of this enamel
type is rather irregular, with no recognizable structural
“units”. Prisms depart from the EDJ parallel to each other
and immediately join to form bundles of varying thickness
that interweave in all the three directions (Fig. 4A, B1). On
the average bundles are 15–20 prisms thick. However, the
number of prisms along each bundle is not constant, as single
prisms may leave one bundle to join another after changing
direction. The thickest and predominant bundles are those
rising to the occlusal surface at 45°–50° (Fig. 4B1). These
bundles usually maintain their orientation throughout the en−
tire thickness of the 3−D enamel zone and pass, without devi−
ating, into successive enamel zones characterized by differ−
ent enamel types. A second set of bundles is directed basally
at about 50° (Fig. 4B1). These latter bundles usually maintain
their orientation for short distances, always limited within
the 3−D enamel zone. A third orientation assumed by the
prisms bundles is sub−horizontal and also in this case prisms
maintain this attitude only within the 3−D enamel zone (Fig.
4B1). In sagittal section, regions of about 100 micrometres
height, where all prisms are parallel and are either occlusally
or, less frequently, basally oriented, are found. The bundles
are here particularly extended vertically but yet lack a lateral
continuity (they do not form layers). In thin section, in fact, it
is clearly observable, by slowly changing the focus, and thus
the depth of the observed plane, that adjacent bundles (in
a bucco−lingual direction) possess different orientations.
Prisms associated with 3−D enamel posses a key−hole cross
Hunter−Schreger bands.—The frequency of successive
HSB and the sinuosity of each band vary on their way to the
outside. In sagittal sections HSB are initially densely packed
and markedly undulated. HSB frequency then quickly de−
creases while the course of the bands become rather straight
or only slightly undulated, rising toward the occlusal surface
(Fig. 4B2). In tangential section the bands are always wavy.
Borders between bands may be either sharp or more or less
fuzzy. Seen at the SEM each band corresponds to a layer of
equally oriented prisms, at an angle with those within adja−
cent layers (horizontal decussation; Fig. 4C). Prisms within
bands are occlusally oriented, rising at about 60°. Individual
HSB shows varying thickness as variable is the angle of
decussation which is, generally speaking, low. Prisms cross
section displays mostly the ginko−leaf morphology.
Radial enamel.—This is formed by parallel prisms, directed
radially away from the EDJ. In M. meridionalis three differ−
ent subtypes of radial enamel are found. The first subtype (A)
is characterized by prisms rising toward the occlusal plane
386 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
FERRETTI—STRUCTURE AND EVOLUTION OF MAMMOTH MOLAR ENAMEL 387
10 mµ30 mµ
30 mµ30 mµ
10 mµ30 mµ
Fig. 3. Variability of the enamel prism cross−sections in the molars of Early Pleistocene southern mammoth, Mammuthus meridionalis (Nesti); Upper
Valdarno, Italy. A. IGF 13730a; M2. A1. Sagittal section of inner enamel layer with prisms showing a keyhole cross−section. A2. Horizontal section of mid−
dle enamel layer; prism cross−sections show a ginko−leaf pattern. A3. Horizontal section of outer enamel layer with prisms showing arch−shaped cross−sec−
tions and frequent fusion with adjacent prisms. B. IGF 13730b; M3. B1. Tangential section of enamel outer layer, near the ECJ, showing prisms with square
cross−sections, surrounded by abundant IPM. B2. Orientation as in D, but at higher magnification, showing the thick interprismatic matrix (IPM) between
the prisms (P). IPM cristallites are parallel to the prisms. C. IGF 1147; M3; oblique section through enamel middle and outer layers showing how prism
cross−sections vary from the EDJ (top, left) to the OES (bottom, right).
388 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
Fig. 4. Enamel types in the molars of Early Pleistocene southern mammoth, Mammuthus meridionalis (Nesti); Upper Valdarno, Italy. A. IGF 13730a; M2,
tangential section of enamel at the EDJ, viewed toward the OES; occlusal surface at top; almost all prisms are sectioned perpendicularly to their long axis
and are irregularly packed. B. IGF 13730b; M3. B1. Sagittal section of inner enamel layer made up of 3−D enamel; arrows show the directions of three prism
bundles surrounding a central triangular area with prisms directed perpendicularly to the figure plane; occlusal surface at top. B2. Reflected light micrograph
of the same sample as in B1; occlusal surface at top; the optic−fiber effect of prisms evidences the complex structure of the inner enamel layer, along the EDJ,
and the wavy HSB in the middle layer. The OES, in contact with the cement (c), is particularly irregular. C. Sagittal section of enamel middle layer com−®
with an angle of about 60° (Fig. 4D1). Prism outline varies
from the ginko−leaf pattern to the key−hole one.
In the second subtype (B), prisms are sub−parallel to the
occlusal surface and normal to the enamel outer surface
(Fig. 4D1), possessing an irregular key−hole transverse sec−
tion (Fig. 3A3). The transverse diameter of the prisms form−
ing radial enamel subtype B is greater than in the previous
enamel types and the apparent fusion (see paragraph on
Prism cross section) between contiguous prisms is frequent
(Fig. 3A3, C). IPM is absent. The third radial enamel subtype
(C) is also characterized by prisms parallel to the masticatory
surface, but prism cross section narrows and becomes sub−
circular. The prismatic sheath may either completely sur−
round the prisms or be open basally (Fig. 3B1, B2).
Prismless enamel.—This type lacks a prismatic organiza−
tion and is composed by a matrix of apatite crystallites paral−
lel to each other (Fig. 4D2). However, average crystallite ori−
entation is locally variable (see below).
Distribution and variability of enamel types
Schmelzmuster.—The schmelzmuster of M. meridionalis
molars is three−layered (Fig. 5). The innermost layer, in con−
tact with the dentine, is formed by 3−D enamel. It represents
about 15–20 per cent of the entire enamel thickness. The mid−
dle layer makes up almost 50–60 per cent of the total enamel
thickness and has two zones: in an innermost zone the enamel
is formed by HSB; the outermost zone consists instead of ra−
dial enamel. The transition between these two enamel types is
rather gradual. Passing from the zone with HSB to that with ra−
dial enamel, prism decussation weakens and eventually
prisms become parallel to each other. On the contrary the
boundary between the middle and the third, outermost layer, is
marked by a sudden flattening of the inclination of the prisms,
which become parallel to the occlusal plane (Fig. 4D1). The
outermost layer can be divided, however, into two rather dis−
tinct zones: (1) an innermost one characterized by prisms
showing a key−hole cross−section and without IPM (radial
enamel subtype B), and (2) an outer zone exhibiting prism
with a rounded cross−section and abundant IPM (radial
enamel subtype C). The outermost layers constitutes, on the
average, about 21 per cent of the enamel thickness. In almost
all the samples a thin layer of prismless enamel occurs near the
OES. This last enamel type will be discussed further below.
Intraspecific variability.—Analysis of an unworn molar plate
(IGF 13730b) showed that the schmelzmuster of M. meridio−
nalis varies along the height of the crown. The enamel capping
the plate tubercles does not have the inner 3−D enamel layer and
consists of only two layers. The innermost zone of the inner
layer is composed, instead, by thin HSB (Fig. 6A1,A
in concentric layers around the tubercles’ vertical axis. More
outwardly the HSB give place to a zone of radial enamel (sub−
type A). A simultaneous bend of the prisms from a steeply ris−
ing direction to a nearly horizontal one, produces a thick outer
layer formed by radial enamel subtype B. Further down, about
20 mm from the tubercle tips, the enamel displays the three−lay−
ered schmelzmuster, as described in the previous section. The
same vertical variation is found in Loxodonta africana (speci−
men KOE 164) and has been described in Elephas recki
brumpti Beden, 1980 by Bertrand (1987). The entire sample of
M. meridionalis teeth, both uppers and lowers, examined in this
study, adheres to this schmelzmuster. The only noticeable dif−
ference was found in the dp3 (specimen IGF 145), that shows a
stronger decussation of the HSB (Fig. 6B). On the other hand,
the dp4 (specimen IGF 157) is characterized by HSB with a
lower angle of decussation, comparable to that of the adult
molars (M1, M2, and M3).
Specimen IGF 13730a is a molar fragment formed by the
posterior enamel crest of a plate and the anterior one of the
succeeding one. No differences in thickness and micro−
structure between the two enamel crests were detected.
In thin section the Striae of Retzius are clearly visible. They
are nearly parallel to the EDJ (Fig. 6C). Each stria represent
FERRETTI—STRUCTURE AND EVOLUTION OF MAMMOTH MOLAR ENAMEL 389
posed by weekly decussating horizontal prisms layers (HSB): a, b label bands with prisms running, respectively, occlusally and labially (intersecting the fig−
ure plane), and occlusally and parallel to the figure plane; EDJ at left, occlusal surface at top. D. IGF 69; m3. D1. Sagittal section of enamel showing the
boundary between middle (left) and outer (right) enamel layers, marked by the simultaneous bending of prisms (at center); EDJ at left, occlusal surface at
top. D2. Sagittal section of the same, outer enamel layer, near the OES; EDJ at left, occlusal surface at top; between radial enamel subtype B (left) and PLEX
(right) there is a narrow transitional zone made up by radial enamel with thick IPM (subtype C; at center).
layer middle layer outer
Fig. 5. Schematic representation of a sagittal section of upper molar enamel
of M. meridionalis, based on Fig. 4B2. Boundaries between inner, middle,
and outer enamel layers are shown by vertical dotted lines.
the position of the enamel growth front in correspondence of
periodical interruptions or slowing down of the mineraliza−
tion process. The contrast between light and dark bands
seems due to a different degree of mineralization of the
enamel (see Carlson 1995 for a review). The incremental
lines seen in M. meridionalis enamel are characterized by
variable thickness. They met the OES at a very low angle.
Prisms themselves present along their longitudinal aspect
periodic micro−variations of crystallite orientation that give
origin to a series of varicosities, analogous to that described
in human enamel (Schroeder 1992). These structures are also
related to the accretionary rate, but of shorter period, possi−
bly daily (Boyde 1976), with respect to the striae of Retzius.
Prismless enamel and the enamel−cement
The OES, covered by cement, is extremely wrinkled. (Figs.
4B2, 6C). This roughness is determined by (1) vertical undula−
tions (parallel to the plate vertical axis), affecting, at variable
depth the entire enamel band, and (2) small rounded protuber−
ances, affecting only the outer portion with prismless enamel.
Under the light microscope these protuberances are visible, in
sagittal section, as marked, sometimes drop−like, convexity of
the ECJ. As a result, the ECJ appears extremely indented (Fig.
6C). As a consequence there is a deep interlocking of the
enamel outer surface with the cement layer. Observed under
390 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
Striae of Retzius
Fig. 6. Enamel types and growth structures in the molars of early Pleistocene southern mammoth. A,B.Mammuthus meridionalis (Nesti); Upper Valdarno,
Italy. A. IGF 13730b; M3. A1. Reflected light micrograph of a sagittal section of a molar plate tubercle, showing thin HSB in the innermost portion of
enamel; occlusal end at top. A2. SEM micrograph of the same sample as in A1, showing the thin, straight and only slightly decussating HSB. B. IGF 145;
dp3, sagittal section of the middle enamel layer made up by strongly decussating HSB; EDJ at left, occlusal surface at top. C. Schematic representation of a
sagittal section of upper molar enamel of M. meridionalis, based on a thin section prepared from specimen IGF 13730b. The drawing outlines a set of incre−
mental lines (striae of Retzius) in the center of the middle enamel layer. Morphological details of the OES are showed.
high resolution polarized light, the enamel can be seen to
bulge along the ECJ, and it is possible to note that crystallites
are not parallel, as in the rest of the prismless enamel zone, but
radially oriented, around the bulge’s symmetry axes. More−
over, incremental lines, visible in some cases, evidence an
arch−shaped growing front for the bulges. These observations
seem to suggest that the occurrence of such an external enamel
zone, which lacks a prismatic organization, is essential to the
development of the rough OES.
Enamel occlusal surface
The wear−induced occlusal surface (secondary surface) of ele−
phant (subfamily Elephantinae, sensu Maglio 1973) molars is
not perpendicular to the tooth vertical axis, but rather mesially
sloping in both upper and lower molars (actually, in lower mo−
lars this is the case when they are at an intermediate stage o
wear). The enamel band of each plate is sectioned on the
occlusal plane and gives origin to two transverse crests, dis−
tally inclined in upper molars, and normal to distally inclined
in the lower ones (Fig. 7). In the molars of this sample, the
enamel crests have a round sagittal section due to polishing
from food items and repeated contact with opposing enamel
crests during occlusion. The prevalent direction of the power
stroke in the mastication process is revealed by the dentine and
cement profile, as observable in sagittal sections (cf.
Koenigswald et al. 1994). In the lower molars of the sample,
dentine and cement between enamel crests are more excavated
in a distal direction. The reverse occurs in the upper molar
(Fig. 7). It follows that in Mammuthus, as it is generally ac−
cepted for recent elephants, mastication is mostly unidirec−
tional. In particular the power stroke direction is horizontal
and forward. This determines the leading and trailing edges
(Greaves 1973; Costa and Greaves 1981), that correspond, re−
spectively, to the plate mesial and distal enamel crests in lower
molars and to the distal and mesial ones in upper molars (Fig.
7). As already reported above, the leading and trailing crests
have the same schmelzmuster in M. meridionalis, and do not
differentiate in thickness. However, because of the symmetry
between the leading and trailing enamel crests with respect to
the plate’s dentine core, the enamel prisms of the two crests
are directed in opposite directions. In particular, in the central
and most elevated portion of the leading crest, corresponding
to the enamel middle layer, prisms meet the surface at an angle
and are oriented opposite to the chewing direction. In the
trailing crest prisms are also occlusally directed, but point
toward the chewing direction (Fig. 8).
Diagenetic alterations of the enamel
The high stability of apatite makes enamel particularly resis−
tant to diagenetic processes. This is testified by the SEM mi−
crographs which show that microstructural features of the
fossil samples are perfectly preserved. This is further proven
by comparison with recent material of E. maximus and L.
africana. For these reasons all the features of M. meridio−
nalis enamel so far described are here considered as “pri−
mary”. Nevertheless, enamel of M. meridionalis presents of−
ten, in correspondence to the outermost layer, a brownish
coloration, very evident in thin section, where it contrasts
with the transparent inner layers. In polarized light this layer
assumes the typical colors of iron (Fe) minerals. A com−
positional micro−analysis with a microprobe confirmed the
FERRETTI—STRUCTURE AND EVOLUTION OF MAMMOTH MOLAR ENAMEL 391
dentine enamel cemen
trailing crest leading crest
me me me
me me di
me: mesial enamel bandplate
di: distal enamel bandplate
Fig. 7. Schematic representation of the sagittal section of opposite Mam−
muthus molars, showing details of the occlusal surface.
direction of enamel
prisms in the middl
Fig. 8. Schematic representation of the sagittal section of the leading and
trailing enamel crests of a lower molar plate, showing the convex outline of
the enamel crests, the direction of enamel prisms (arrows) in the middle
enamel layer, and the chewing direction. The latter is determined by the rel−
ative movement of the opposite teeth during mastication.
of enamelM. Meridionalis
Rate = 1237 CPS
54 CNT 6. 76KEV 10eV/ch B EDAX
Fig. 9. Chemical compositional microanalysis of M. meridionalis enamel
(IGF 13730b). The analysis of the outer enamel layer revealed, beside the
presence of calcium (Ca) and phosphate (P), the occurrence of iron (Fe) and
manganese (Mn), interpreted as diagenetic secondary elements. The chlo−
rine (Cl) signal is due to the use of HCl to etch the enamel section. CPS,
counts per second.
occurrence of Fe and manganese (Mn) within the outer
enamel layer in two sample of M. meridionalis (Fig. 9). On
the other hand, no traces of Fe have been found in the middle
and inner layer of the same samples or at any location in the
enamel samples of E. maximus or L. africana.
Enamel differentiation in Mammuthus
Both the studied molars of late Middle Pliocene M. rumanus
from Montopoli and late Early Pleistocene M. meridionalis
from Farneta and Pietrafitta show the same schmelzmuster as
the specimens from Upper Valdarno (early Early Pleisto−
cene). M. trogontherii and M. primigenius are also character−
ized by the same schmelzmuster of M. meridionalis and M.
rumanus, even though they possess thinner enamel. On the
other hand the molars of the four mammoth species exam−
ined differ in the relative thickness of the three enamel layers.
Table 2 reports the mean percentage thickness (see Meth−
ods) of the three enamel layers in the M3 of M. rumanus,M.
meridionalis,M. trogontherii, and M. primigenius. Given the
small number of specimens for each species, data should be
evaluated with caution, however the results are consistent
and allow some functional interpretations (see Discussion).
The inner layer constitutes, in the first three species men−
tioned above, approximately 15 per cent of the whole enamel
thickness. In M. primigenius the inner enamel is thinner than
in the three older species, representing from 6 to 10 per cent
of the whole thickness. The middle layer is, on the contrary,
significantly (P <0.05) thinner in M. meridionalis (62 per
cent) and thicker in M. primigenius (75 per cent). Accord−
ingly the outer enamel layer become relatively thinner pass−
ing from the oldest (M. rumanus; 31 per cent) to the youngest
(M. primigenius; 16 per cent) species (Fig. 10).
Discussion and conclusions
Structure and function
This analysis reveals that molars of Eurasian Mammuthus
species are characterized by a schmelzmuster composed by
four main enamel types, with three radial enamel subtypes.
Two major discontinuities delimit three layers: in an inner−
most layer the enamel is formed by a complex enamel type,
termed 3D enamel by Pfretzschner (1994); the middle layer
has occlusally rising prisms, organized into HSB in an inner−
most zone and into radial enamel, with occlusally rising
prisms, in an outermost one; the outermost layer is built up
by radial enamel with nearly horizontally oriented prisms,
and a thin outer zone of a prismless enamel, in contact with
the cement cover. This latter, “primitive” enamel type, which
in mammals is frequently formed when ameloblast activity is
ending (Boyde 1964; Schroeder 1992), and constitutes the so
called prismless external layer (PLEX; Martin 1992), is
found both in M. meridionalis and in the two extant species
E. maximus and L. africana. PLEX seems thus to represent a
constant component of the schmelzmuster of elephants too. It
was also observed in the Eocene proboscidean Numido−
therium koholense Mahboubi et al., 1986 (Numidotheriidae)
from the Eocene of Algeria (Bertrand 1987). It is here sug−
gested that PLEX, forming the extremely rough OES,
increases adhesion of the crown cement.
While HSB, radial, and prismless enamel are common
among placental mammals, 3−D enamel is restricted to the
392 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
Table 2. Enamel thickness differentiation in the upper M3 of four successive Eurasian Mammuthus species.
Relative enamel thickness (%) Enamel thickness (mm)
Inner layer Middle layer Outer layer
N mean min–max mean min–max mean min–max N mean min–max
M. rumanus Montopoli 1 15 – 54 – 31 – 2 3.5 3.2–3.9
M. meridionalis Upper Valdarno and Farneta 3 17 13–21 62 55–67 21 18–24 43 3.2 2.6–3.9
M. trogontherii Süssenborn 1 13 – 66 – 21 – 46 2.3 1.9–3.0
M. primigenius Sickenhofen and Arezzo 2 9 6–10 75 71–79 16 13–23 3* 1.9 1.5–2.3
*material from Arezzo, Italy (IGF).
Arezzo and Sickenhofen
0 100 %
inner layer middle layer outer layer (%)
Fig. 10. Enamel thickness differentiation in four successive European
mammoth samples. Descriptive statistics are given in Table 2.
Proboscidea. It can be defined as an irregular enamel, follow−
ing the definition by Koenigswald and Sander (1997c) and
was called 3−D enamel by Pfretzschner (1994) because it
contains prism bundles running in all the three directions of
space. 3−D enamel is found adjacent to the EDJ, where inten−
sity of shear forces produced during occlusion are higher and
shear forces are oriented in the three directions of space
(Pfretzschner 1992, 1994). The complex structure of 3−D
enamel seems thus a mechanical adaptation to withstand this
stress pattern. Other mammals with hypsodont molars (e.g.,
Equus caballus,Phacochoerus aethiopicus,Bos taurus) also
developed specialized enamel types near the EDJ, that,
though structurally different, are functionally similar to 3−D
enamel (Pfretzschner 1992, 1994). 3−D enamel is not present
in the enamel capping the plate tubercles, where a two−lay−
ered enamel occurs. HSB are instead encountered in an in−
nermost zone. This simplified schmelzmuster has been found
also in Elephas recki and Loxodonta africana at the same lo−
cation, which indicates this is a pattern typical for Elephan−
tinae. A similar two−layered schmelzmuster characterizes the
enamel of the Eocene proboscidean Moeritherium lyonsi An−
drews, 1901 (Moeritheriidae) (Bertrand 1987; Ferretti un−
published data) and is therefore believed to be the plesio−
morphic condition for Proboscidea. The occlusal end of an
unworn elephant plate thus exhibits plesiomorphic features
in both its gross morphology (i.e., subdivision in tubercles)
and microstructure, relative to the rest of the plate. From this
it also follows that increment of crown height, a trend charac−
terizing elephant evolution, involves extension of the onto−
genetic phase when the central portion of the tooth crown is
formed. The same pattern has been demonstrated for hypso−
dont representatives of the Arvicolidae (Koenigswald 1993;
Koenigswald and Kolfschoten 1996).
The predominant prism type in Mammuthus enamel is the
type 3, or key−hole pattern, while a thin zone of an irregular
type, intermediate between type 1 and 3, is confined to the
outermost layer. Prism cross−sections, thus, varies from an
open prism sheath to a closed prism sheath, along their
course from the EDJ to the OES. Bertrand (1987, 1988) re−
ports the occurrence of type 1 enamel close to the EDJ in two
Eocene species from Pakistan of the basal proboscidean fam−
ily Anthracobunidae, in N. koholense, and in a molar of an
unidentified species of Palaeomastodon Andrews, 1901
from the Oligocene of Egypt. However, all the specimens ex−
amined in the present study have type 3 prisms at the EDJ.
Within each plate there is no differentiation of the enamel
between “leading” and “trailing” enamel crest, even though
the prevalently protinal (i.e., forwardly directed; Koenigs−
wald et al., 1994) mastication of elephantids (Elephantidae,
sensu Maglio 1973) should in theory produce different me−
chanical stress on the mesial and the distal enamel band of a
plate (cf. Koenigswald 1980; Pfretzschner 1994). However,
if enamel microstructure actually reflects stress direction and
intensity, one would presume that in the molars of the inves−
tigated Mammuthus species these should be the same on both
enamel crests (cf. Rensberger 1995b). Enamel differentiation
between leading and trailing crests is observed usually in
species with very thin enamel (e.g., rodents), a characteristic
that strongly constrains enamel microstructure (cf. Koenigs−
wald and Sander 1997b). It can be argued that the relatively
thick enamel of elephants (from 1 to 5 mm) guarantees an ad−
equate robustness to both enamel crests, even though they
may be subject to different tensile stresses.
All the studied cheek teeth of M. meridionalis present the
same schmelzmuster. Only the dp3 is different in having
stronger decussating HSB. As higher angles of decussation
reinforce enamel to withstand fracture (Koenigswald and
Pfretzschner 1987; Pfretzschner 1988) this could represent
an adaptation to strengthen the relatively thinner enamel of
the dp3 (about 1 mm).
A characteristic of the dental evolution of Eurasian Mam−
muthus is the progressive reduction of enamel thickness (Lis−
ter 1996; Maglio 1973; Aguirre 1969). From the present
study it is concluded that a thinner enamel evolved in late
Mammuthus species through a progressive shortening of the
period of formation of the enamel band during tooth onto−
genesis (see Martin 1985), and not by losing one or more
enamel zones, as is the case in some rodent lineages
(e.g., Microtus and Arvicola; Koenigswald 1980). The
schmelzmuster maintained, in fact, the same structural char−
acteristics along the Eurasian mammoth line. On the other
hand, evidence presented in this study indicates that, along
with the enamel thinning trend, the relative thickness of the
three layers constituting the mammoths’ enamel underwent a
differential modification. In particular the relative thickness
of the outermost layer, where enamel prisms are parallel to
the occlusal surface and thus offer a lesser resistance against
wear (Rensberger and Koenigswald 1980), decreased in the
transition from M. rumanus to M. primigenius (Fig. 10). In
contrast, the middle layer, which is made up by prisms set at
an angle with the occlusal surface (an attitude that makes
enamel more resistant to wear) increased its relative thick−
ness. The enamel differentiation observed in the Eurasian
mammoth line could represent an adaptation to keep the rate
of wear to a minimum as the enamel became thinner and/or
the diet more abrasive. To corroborate this hypothesis, how−
ever, additional data are needed. It would also be of great
interest to investigate whether the American Mammuthus
lineage (M. “hayi” – M. imperator –M. columbi), that also
evolved thin−enameled hypsodont molars (Madden 1981),
underwent similar microstructural changes.
The presence of iron demonstrated in many M. meridionalis
enamel samples and its absence in those from extant species,
would suggest a secondary, i.e., diagenetic, origin of the iron,
an hypothesis that is supported here. This hypothesis, how−
ever, does not easily explain why the iron−bearing layer ex−
FERRETTI—STRUCTURE AND EVOLUTION OF MAMMOTH MOLAR ENAMEL 393
actly matches with the enamel outer layer and no traces of
iron has been revealed in the middle layer. The outer layer is
made up mostly by a radial enamel with prisms wider than in
the remainder of the enamel. If there is a relationship be−
tween iron enrichment and enamel structure, it must be sup−
posed that the radial enamel forming the outermost layer is
somehow more permeable to Fe ions than the other enamel
types occurring in M. meridionalis.
Kamiya (1981), in a study on the alteration of the enamel in
E.(Palaeoloxodon)naumanni Makiyama, 1924, considers the
occurrence of prisms with badly defined outlines and of areas
with prismless enamel near the OES, as modification of the
apatite crystals due to diagenetic processes. From the figures
and description of Kamiya, the supposed altered areas in E.
(P.) naumanni enamel show similarities, respectively, with the
radial enamel with IPM (subtype C) and to the PLEX found in
M. meridionalis. The numerous observations made in the
present analysis and comparisons with enamel of the extant
species, however, strongly support the opinion that in M.
meridionalis, these are primary features of the enamel.
Enamel structure and proboscidean systematics
Mammuthus species possess the same schmelzmuster in all
their cheek teeth. The analysis revealed some minor differ−
ences among specimens, including the complexity of 3−D
enamel, and the thickness of HSB, but at present, due to the
small sample size, these cannot be distinguished from indi−
vidual variability. It is important to distinguish the portion of
the tooth crown being examined, since the apicies of the tu−
bercles display a simpler structure, as opposed to that of the
rest of the molar plate. The other elephant taxa examined (E.
maximus and L. africana) exhibit the same microstructural
pattern, further supporting the conclusion that in the cheek
teeth of Elephantinae no structural differentiation exists. On
the other hand the observed thickness differentiation in the
Eurasian mammoth lineage would indicate that differential
relative thickness of the enamel layers could represent a use−
ful diagnostic character for intrageneric systematics. Prelimi−
nary comparison, as part of an ongoing work, with represen−
tatives of the principal proboscidean clades (Fig. 11) sug−
gests that the occurrence, in the central portion of the tooth
crown, of 3−D enamel and a schmelzmuster composed by six
enamel types and subtypes (3−D enamel−HSB−radial enamel
subtypes A, B, and C−prismless enamel) are synapomorphies
of the Elephantoidea (sensu Tassy 1990). This complex
schmelzmuster developed from a more simple one, like that
found in the Eo–Oligocene Moeritherium lyonsi (Bertrand
1987, 1988; Pfretzschner 1994). The early diverging families
Numidotheriidae, Barytheriidae, and Deinotheriidae devel−
oped, possibly from a moerithere−like pattern, a specialized
enamel made up almost entirely by 3−D enamel (Remy 1976;
Bertrand 1987; Koenigswald et al. 1993; Pfretzschner 1994).
Representatives of the Early Oligocene genus Palaeo−
mastodon, the sister taxon of all Neogene elephantoids
(Tassy 1990), display an intermediate condition between
those of the latter group and M. lyonsi (Bertrand 1997;
Pfretzschner 1994). From these results it appears that enamel
structure in proboscideans may represent an important tool
for ingroup systematics at the species and family level.
I thank Giovanni Ficcarelli and Lorenzo Rook (Florence) for help and
critical reading of the manuscript. Raymond Bernor (Washington) is
acknowledged for critically reading an earlier draft of the manuscript
and for improving the English text. I am grateful to Wigarth von
Koenigswald, Martin Sanders, Hans Ulrich Preftzschner, and Elke
Knipping for help and discussion during my visit to the Institute für
Paläontologie of the University of Bonn in 1994. I am indebted to
Wigarth von Koenigswald for providing me with various proboscidean
enamel samples. I thank Ralph D. Kahlke and Lutz Maul (Weimar) for
the M. trogontherii specimen. I am grateful to Adrian Lister (London)
for suggestions and insights. Finally, this work benefits from the exper−
tise of many colleagues at the University of Florence: Elisabetta Cioppi
(fossil collection), Francesco Landucci (photography), Maurizio Ulivi
and Mauro Paolieri (SEM). Financial support for this research has been
provided by the University of Florence and the Italian Ministry of
Education, University, and Scientific Research (MIUR).
394 ACTA PALAEONTOLOGICA POLONICA 48 (3), 2003
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