Journal of Human Evolution 74 (2014) 96e113
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Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol
The late Early Pleistocene human dental remains from Uadi Aalad and
Mulhuli-Amo (Buia), Eritrean Danakil: Macromorphology and
microstructure
Clément Zanolli a, *, Luca Bondioli b, Alfredo Coppa c, Christopher M. Dean d,
Priscilla Bayle e, Francesca Candilio c, Silvia Capuani f, Diego Dreossi g, Ivana Fiore c,
David W. Frayer h, Yosief Libsekal i, Lucia Mancini g, Lorenzo Rook j, Tsegai Medin Tekle i, k,
Claudio Tuniz a, c, l, Roberto Macchiarelli m, n
a
Multidisciplinary Laboratory, The ‘Abdus Salam’ International Centre for Theoretical Physics, Trieste, Italy
Museo Nazionale Preistorico Etnografico ‘Luigi Pigorini’, Rome, Italy
c
Dipartimento di Biologia Ambientale, Università di Roma ‘La Sapienza’, Rome, Italy
d
Department of Cell and Developmental Biology, University College London, UK
e
UMR 5199 PACEA, Université Bordeaux 1, France
f
CNR-IPCF, Dipartimento di Fisica, Università di Roma ‘La Sapienza’, Rome, Italy
g
Elettra-Sincrotrone Trieste S.C.p.A., SYRMEP Group, Basovizza, Italy
h
Department of Anthropology, University of Kansas, Lawrence, USA
i
National Museum of Eritrea, Asmara, Eritrea
j
Dipartimento di Scienze della Terra, Università di Firenze, Italy
k
Institut Catala de Paleoecologia Humana i Evolució Social, Universitat Rovira i Virgili, Tarragona, Spain
l
Centre for Archaeological Science, University of Wollongong, Australia
m
Département de Préhistoire, UMR 7194, MNHN, Paris, France
n
Département Géosciences, Université de Poitiers, France
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 10 November 2013
Accepted 22 April 2014
Available online 19 May 2014
Fieldwork performed during the last 15 years in various Early Pleistocene East African sites has significantly enlarged the fossil record of Homo erectus sensu lato (s.l.). Additional evidence comes from the
Danakil Depression of Eritrea, where over 200 late Early to early Middle Pleistocene sites have been
identified within a w1000 m-thick sedimentary succession outcropping in the Dandiero Rift Basin, near
Buia. Along with an adult cranium (UA 31), which displays a blend of H. erectus-like and derived morphoarchitectural features and three pelvic remains, two isolated permanent incisors (UA 222 and UA 369)
have also been recovered from the 1 Ma (millions of years ago) Homo-bearing outcrop of Uadi Aalad.
Since 2010, our surveys have expanded to the nearby (4.7 km) site of Mulhuli-Amo (MA). This is a
fossiliferous area that has been preliminarily surveyed because of its exceptional concentration of
Acheulean stone tools. So far, the site has yielded 10 human remains, including the unworn crown of a
lower permanent molar (MA 93). Using diverse analytical tools (including high resolution mCT and mMRI),
we analysed the external and internal macromorphology and microstructure of the three specimens, and
whenever possible compared the results with similar evidence from early Homo, H. erectus s.l.,
H. antecessor, H. heidelbergensis (from North Africa), Neanderthals and modern humans. We also assessed
the UA 369 lower incisor from Uadi Aalad for root completion timing and showed that it compares well
with data for root apex closure in modern human populations.
Ó 2014 Elsevier Ltd. All rights reserved.
Keywords:
Buia
Homo erectus/ergaster
East Africa
Teeth
External morphology
Internal structure
Introduction
* Corresponding author.
E-mail address: [email protected] (C. Zanolli).
http://dx.doi.org/10.1016/j.jhevol.2014.04.005
0047-2484/Ó 2014 Elsevier Ltd. All rights reserved.
Geological, paleontological and paleoanthropological field
research has been carried out in the Dandiero Rift Basin, northern
Danakil Depression of Eritrea since 1994. This research has led to
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
the discovery of over 200 late Early to early Middle Pleistocene sites
with widespread evidence of vertebrate faunal remains and lithic
artefacts within the nearly 1000 m-thick fluvio-deltaic-lacustrine
sedimentary succession outcropping 100 km south of Massawa
(Abbate et al., 1998, 2004; Ghinassi et al., 2009; review in; Rook
et al., 2012). Thus far, in an area covering about 40 km2, cranial,
dental and postcranial human remains have been discovered in two
localities near the Buia village: Uadi (Wadi) Aalad and Mulhuli-Amo
(Coppa et al., 2012).
The continental basin fill (the so-called Maebele Synthem)
consists, from bottom to top, of six lithostratigraphic units: fluvial
Bukra sand and gravel, fluvio-deltaic Alat Formation, fluvial Wara
sand and gravel, lacustrine Goreya Formation; fluvio-deltaic Aro
sand; and alluvial fan Addai fanglomerate (Abbate et al., 2004;
Papini et al., 2014). The Homo-bearing deposits belong to the upper part of the 70e100 m-thick fluvio-deltaic Alat Formation
(Ghinassi et al., 2009).
The upper part of the Alat Formation hosts the top of the Jaramillo subchron (0.99 Ma), which occurs about 10 m below the
transition to the overlying Wara sand and gravel. The MatuyamaBrunhes boundary (0.78 Ma) is located about 5 m above the base
of the Aro sand unit (Albianelli and Napoleone, 2004). Confirmation
of the magnetostratigraphically-based chronological setting comes
from fission track dating (Bigazzi et al., 2004) and mammal biochronology (Ferretti et al., 2003; Martínez-Navarro et al., 2004,
2010; Rook et al., 2010, 2012).
All human remains discovered so far occur in the upper part of
the Alat Formation, where the transition from a deltaic to alluvial
setting is characterized by high frequency, potentially millennialscale, lake-level oscillations (units DL5, FL2a and FL2b in Ghinassi
et al., 2009). Specifically, the concentration of fossil bones at the
base of the FL2b was associated with an increase in fluvial discharge
that caused winnowing of the immediately underlying fossilbearing fluvio-deltaic deposits. As a whole, both the sedimentary
record documenting the evolution of fluvio-deltaic and lacustrine
systems (Ghinassi et al., 2009; Rook et al., 2012), and the vertebrate
faunal assemblages predominated by taxa known for their water
dependence (Delfino et al., 2004; Martínez-Navarro et al., 2004),
clearly indicate a relatively open paleoenvironmental scenario
characterized by the presence of moist grassed habitats adjacent to
persistent water (Rook et al., 2012).
First identified in the Uadi Aalad (UA) site, the 5e6 m-thick
Homo-bearing layer produced a virtually complete adult cranium
preserving the face (UA 31), two permanent incisors (UA 222 and
UA 369), and three pelvic portions (UA 173, UA 405, UA 466)
(Abbate et al., 1998; Macchiarelli et al., 2004a; Bondioli et al., 2006).
Compared with the Indonesian and Chinese Homo erectus sensu
stricto (s.s.) sample (review in Antón, 2003), as well as with African
specimens such as OH 9 and, to a lesser extent, KNM-ER 3733 (Baab,
2008; Rightmire, 2013) and to the chronogeographically close
calvaria from Daka, Middle Awash (Gilbert and Asfaw, 2008), UA 31
displays a blend of H. erectus/ergaster-like and derived morphoarchitectural features more commonly found in Middle Pleistocene specimens. These features include a high positioning of the
maximum parietal breadth, weak parietal keeling along the
midline, slight parasagittal flattening, and from sub-vertical to
slightly downwards converging parietal walls, documenting
extensive variation in late Early Pleistocene East African Homo
(Macchiarelli et al., 2004a).
Since 2010, the systematic survey of a fossiliferous area near to
the exceptionally preserved A006 site (the so-called ‘handaxes
esplanade’) previously reported for its extensive concentration of
Oldowan and Acheulean lithic tools (Martini et al., 2004), has led to
the discovery of new fossil human remains at the Mulhuli-Amo (MA)
locality, 4.7 km south of the UA Homo site (Coppa et al., 2012, 2014).
97
The nearly 15 m-thick sedimentary succession of Mulhuli-Amo
consists of deltaic and fluvial sediments. The lower interval (ca. 5
m) consists of a sandy Gilbert-type delta deposit. The middle interval (5 m) is made of pedogenized muddy deposits with isolated
sandy fluvial channels responsible for the transport and accumulation of bone remains and stone tools in their basal parts. Finally,
the 5 m-thick upper interval of the succession consists of fluvial
channelized gravelly sand capped with pedogenized mud. Even if
most fossil remains from this site are spread on the eroded surface,
most of the bones and Acheulean artefacts occur in situ at the base
of the third interval.
The human fossil-bearing levels of Uadi Aalad and Mulhuli-Amo
are remarkably similar in sedimentary facies and depositional
history (cf. Ghinassi et al., 2009; Rook et al., 2012), and are
considered to sample the same stratigraphic horizon belonging to
the Alat. Besides the presence of reptile remains including crocodiles (Crocodylus niloticus), turtles (Pelusios sinuatus), and monitor
lizards (Varanus niloticus), the vertebrate assemblage at MulhuliAmo consists of the same mammal taxa represented at Uadi
Aalad (i.e., Elephas, Hippopotamus, Kolpochoerus, Kobus, Pelorovis).
A total of 10 cranial and dental human remains, likely from two
adults and one immature individual, have been collected so far at
Mulhuli-Amo. They consist of an isolated frontal fragment bearing a
thick right torus (MA 14) and eight parietal fragments (MA 64 and
MA 88aef) associated with a temporal bone fragment (MA 89), all
from a single adult cranium showing structural (thickness distribution) and architectural features (proportions, curvature) closely
fitting the morphology represented by UA 31. Finally, the assemblage includes an isolated permanent lower molar crown (MA 93)
(Coppa et al., 2014).
Compared with the Southeast Asian and Indonesian hypodigm
(Indriati, 2004; Kaifu et al., 2005), the human dental assemblage
from chronologically well-constrained Early Pleistocene African
sites (e.g., McDougall et al., 2012) is qualitatively and quantitatively
relatively rich until about 1.4 Ma (millions of years ago) (cf. Wood,
1991), while evidence from the later Early Pleistocene is scanty
(Schwartz and Tattersall, 2003; Suwa et al., 2007; Brink et al., 2012).
The material we examine here thus enlarges this sample and contributes to partially fill the gap still existing between the dental
records available so far for African H. erectus sensu lato (s.l.) on one
hand, and Homo heidelbergensis on the other hand.
Building on the announcement (Abbate et al., 1998) and preliminary general description of the two incisors from Uadi Aalad,
collected in 1995 and 1997, respectively (Macchiarelli et al., 2004a),
and the molar crown from Mulhuli Amo, collected in 2011, here we
provide details of their external and internal morphology. More
specifically, we compare the structure of the three Eritrean specimens sampling H. erectus/ergaster with some earlier and later human taxa, particularly with the evidence from the early Middle
Pleistocene North African sample of Tighenif, using a variety of
investigative approaches and analytical tools granting high resolution access to their microstructure (Zanolli and Mazurier, 2013).
In doing so, we reveal for the first time the primitive versus derived
nature of some tooth structural features in African H. erectus s.l.
near the end of the Early Pleistocene and investigate their evolutionary polarity at a macroregional scale.
Materials and methods
The three fossil teeth from the Buia area represent an upper left
lateral permanent incisor (UA 222) and a lower left central permanent incisor (UA 369) from the Homo site of Uadi Aalad (Abbate
et al., 1998; Macchiarelli et al., 2004a), and a lower left M1/M2
crown (MA 93) from Mulhuli-Amo (Coppa et al., 2012, 2014; Zanolli
et al., 2013). The incisors preserve the crown and root, while the
98
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
molar is represented only by the crown. This material is permanently stored at the Geo-Paleontological Laboratory of the National
Museum of Eritrea.
Outer morphology
The degree of occlusal wear was assessed according to Smith
(1984), with description of the nonmetric crown topography
following Scott and Turner (1997), based on Arizona State University Dental Anthropology System (ASUDAS) scores (Turner et al.,
1991). Maximum mesiodistal (MD) and buccolingual (BL) crown
diameters (in mm) were measured on the original specimens with
Mitutoyo Digimatic calipers (to the nearest 0.1 mm) and then on
the unsmoothed virtual surfaces generated after segmentation of
the microtomographic record of each specimen (see below). Since
the MD dimension of both incisors is affected by interproximal
wear, we limited the comparative analysis to the BL diameter. For
linear measurements, the Eritrean specimens were variably
compared with a number of fossil and recent samples (Table 1).
Crown microwear
Microwear texture analysis was attempted on the three specimens following the standard procedures described by Mahoney
(2006). The teeth were first cleaned with cotton soaked in
alcohol and molds of their crown surfaces were obtained using high
resolution silicone impression material (Zhermack Elite HD). A cast
Table 1
Fossil and recent comparative samples used for crown linear measurements.
Samples
Tooth
H. habilis-rudolfensis
from East Africa (HHR)
UI2
LI1
LMs
UI2
LI1
LMs
UI2
LI1
LMs
African H. erectus/ergaster from
Kenya and Ethiopia (HEA)
H. erectus from Georgia (HEG)
H. erectus from Java (HEJ)
UI2
LI1
LMs
H. erectus from China (HEC)
UI2
LI1
LMs
H. antecessor from Atapuerca
UI2
Gran Dolina (HA)
LI1
LMs
North African H. heidelbergensis from UI2
Tighenif and Rabat (HHNA)
LI1
LMs
UI2
European H. heidelbergensis from
LI1
Atapuerca Sima de
LMs
los Huesos (HHE)
Neanderthals (NEA)
UI2
LI1
LMs
Near Eastern early H. sapiens
UI2
from Qafzeh (NEEHS)
LI1
LMs
European early Upper Paleolithic
UI2
humans (EUPH)
LI1
LMs
Recent (Holocene) humans (RH)
UI2
LI1
LMs
References
Wood, 1991
Stynder et al., 2001
Wood, 1991; Leakey et al., 2012
Wood, 1991
Stynder et al., 2001
Wood, 1991; Suwa et al., 2007
Martinón-Torres et al., 2008
Martinón-Torres et al., 2008
Martinón-Torres et al., 2008;
Lordkipanidze et al., 2013
Grine and Franzen, 1994;
Zanolli, 2013
Stynder et al., 2001
Wood, 1991; Widianto, 1993;
Kaifu et al., 2005; Zanolli, 2013
Wood, 1991
Wood, 1991
Wood, 1991
Bermúdez de Castro et al., 1999
Bermúdez de Castro et al., 1999
Bermúdez de Castro et al., 1999
Martinón-Torres et al., 2008
Stynder et al., 2001
Wood, 1991
Martinón-Torres et al., 2012
Martinón-Torres et al., 2012
Martinón-Torres et al., 2012
Voisin et al., 2012
Voisin et al., 2012
Voisin et al., 2012
Vandermeersch, 1981
Vandermeersch, 1981
Vandermeersch, 1981
Frayer, 1977
Hillson et al., 2010
Frayer, 1977
Frayer, 1977
Frayer, 1977
Frayer, 1977
of each specimen was produced using transparent epoxy resin
(Hardrock 554, Phase Inc.). Positive transparent araldite replicas
were analysed using a stereomicroscope and the patterns of
microstriations evaluated by scanning electron microscopy (SEM)
(EVO 60 Leitz GmbH). For the latter analysis, the replicas were
sputter coated with gold by means of an Emitech K550X system.
However, in contrast with the two incisors, MA 93 did not provide
any observable details.
High resolution magnetic resonance micro-imaging and root growth
assessment
To assess non-destructively the growth-related dentine microstructures (daily von Ebner and long-period Andresen lines) in
subfossil and fossil teeth (Bondioli et al., 2013), we developed a new
magnetic resonance microimaging (mMRI) analytical approach,
based on previous successful high resolution MRI imaging of
modern human teeth (Weiger et al., 2012). Indeed, techniques in
magnetic resonance imaging (MRI) have advanced rapidly in the
past two decades (Haack et al., 1999), and can now be applied in
place of more destructive methods. Magnetic resonance imaging
utilizes the magnetic moment exhibited by many naturally occurring nuclei, with the proton in the hydrogen nucleus being of
particular importance. Protons are highly abundant in all tissues
and have high magnetic resonance sensitivity. Since the composition of most biological tissue is dominated by water, the differences
in the water environment of adjacent tissue structures can be
manipulated by MRI to effectively visualize tissue structure. More
recently, magnetic resonance microimaging (mMRI) methods have
been developed and refined (Callaghan, 1995) to provide images
characterized by a spatial resolution of approximately 100 mm or
smaller. They have been particularly useful for investigating porous
systems (Strange et al., 1993; Allen et al., 1997) and bones (De Santis
et al., 2010; Wehrli, 2013). Specifically, mMRI techniques are able to
retrieve high resolution information about the density, the mean
diameter, and the distribution of microfeatures in porous systems.
Indeed, when the pores of a porous system, like the dentine, are
filled with a liquid containing protons (usually water), it is possible
to obtain indirect information about the microstructural characteristics of this material from the signal of the liquid entrapped in
the microstructures. Currently, MRI is rarely used in dental diagnosis and research mainly because of the very short transverse
relaxation times of the mineralized tooth tissues.
We performed a preliminary validation test on two perfectly
preserved Neolithic permanent teeth (an upper incisor and a
canine), after comparatively assessing their root microstructure
(dentine tubules and Andresen lines) by means of mCT, mMRI and
histology (Bondioli et al., 2013). We applied this technique to
visualize the dentine microanatomy and tentatively assess the
growth pattern in UA 369. To do so, this well preserved lower left
central permanent incisor was immersed in a thin glass walled tube
used to contain samples in nuclear magnetic resonance spectroscopy, which had been filled with distilled water at the temperature
of 18 C. Images of UA 369 were obtained by using Multi Slice Multi
Echo (MSME) imaging sequences with repetition times (TR) equal
to 380.0 ms, echo times (TE) equal to 3.5 ms, field of view (FOV)
equal to 14 14 mm2, matrix 256 256, and number of scans
averaged (ns) equal to 1024. A total of 11 slices were selected of slice
thickness (STH) equal to 200 mm to investigate the central zone of
UA 369 dentine. The in-plane resolution in each image slice was
55 55 mm2.
All measurements were performed on a Bruker 9.4T Avance-400
system located at the Physics Department of the ‘La Sapienza’
University of Rome, operating with a micro-imaging probe (12 mm
internal diameter bore) and equipped with a gradient unit
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Table 2
Linear, surface, and volumetric variables used for assessing internal structural
variation and molar crown tissue proportions.
Variables
c
b
e
AET (¼c/e)
RET (¼100*
AET/(b1/2))
Ve
Vcd
Vcp
Vcdp
Vc
SEDJ
Vcdp/Vc
(¼100*Vcdp/Vc)
3D AET (¼Ve/SEDJ)
3D RET (¼100*3D
AET/(Vcdp1/3))
Definitions
The enamel area assessed on a buccolingual virtual
section (mm2)
The dentine area under the enamel surface on a
buccolingual virtual section (mm2)
The enamel-dentine junction (EDJ) length on a
buccolingual virtual section (mm)
The bi-dimensional average enamel thickness (mm)
The scale-free, bi-dimensional relative enamel
thickness (Martin, 1985)
The volume of the enamel cap (mm3)
The volume of the coronal dentine (mm3)
The volume of the coronal pulp (mm3)
The volume of the coronal dentine, including the
coronal aspect of the pulp chamber (mm3)
The total crown volume, including enamel, dentine, and
pulp (mm3)
The EDJ surface (mm2)
The percent of coronal volume that is dentine and pulp
(%)
The three-dimensional average enamel thickness (mm)
The scale-free three-dimensional relative enamel
thickness (see Kono, 2004; Olejniczak et al., 2008a)
characterized by a maximum gradient strength of 1200 mT/m, and
a rise time of 100 ms.
Root extension rate was calculated from the mMRI images according to the method detailed in Macchiarelli et al. (2006), Dean
(2009), and Dean and Cole (2013), which can be applied to both
fossil and extant human teeth. Continuous data were collected on
the lingual and labial aspects along almost the entire root length of
UA 369. After outlining the main visible growth incremental lines on
the image of this specimen, dentine tubules were traced from the
root surface just beneath the last formed enamel at the cervix (point
A) to a second point 200 mm along the dentine tubules into root
dentine (point B). This thickness of dentine forms at a rate of 2.23e
2.50 mm/day and takes ca. 80e90 days to form (Dean, 1998, 1999,
2012; Dean and Cole, 2013). A line parallel with the orientation of
the growth markers was drawn from the end (point B) of the 200 mm
segment back to the root surface (point C). The distance between
point A and point C represents the length that the root had extended
in ca. 80e90 days. An extension rate was calculated in mm/day for
this distance along the root. This procedure was then repeated such
that point C became point A in each calculation along the root length.
In H. erectus from Java (S7-37), direct measurements of daily
dentine increments in an upper M1 equalled 1.43 mm per day
over the first 50 mm, 2.46 mm per day between 50 and 100 mm,
and 2.71 mm per day between 100 and 200 mm from the cementdentine junction (CDJ) (Dean et al., 2001; Dean, 2009). The overall
mean daily rate over 200 mm of dentine formation from the CDJ
(point A to point B) was 2.4 mm per day in this upper M1, but no
equivalent data exist for anterior teeth in African H. erectus.
Previously, a rate of 2.5 mm per day has been used to calculate 80
days formation for a 200 mm thickness of newly formed root
dentine in modern human teeth. However, Smith et al. (2007)
have argued that in some teeth of Pan troglodytes dentine formation rates average closer to 2 mm per day at the cervix. Dean
(2009) and Dean and Cole (2013) also observed rates of
w2.0 mm per day in some modern human anterior teeth. Because
it remains unclear what the exact range of daily dentine formation rates is likely to have been in UA 369, we have adopted a
cautious approach and have used both 80 and 90 day formation
times (equivalent to 2.2e2.5 mm per day) to provide what we feel
is the most likely range of estimates for the time taken to form
consecutive lengths of root along the CDJ.
99
Microtomographic-based inner structure
The three specimens were detailed using X-ray microtomography (mCT) at the SYRMEP beamline (crown portion of the
tooth) and at the Tomolab station (whole tooth) of the Elettra
Sincrotrone Trieste laboratory (Basovizza, Italy). The measurements
performed on the whole tooth were carried out according to the
following parameters: 100 kV voltage, 80 mA current, 4.0 s exposition time per projection, and a projection each 0.25 , for the incisors; 130 kV, 61 mA, 4.5 s, and 0.15 for MA 93. Their final volumes
were reconstructed with an isotropic voxel size of 10.0 and 8.3 mm,
respectively. Using Amira v.5.3 (Visualization Sciences Group Inc.)
and ImageJ (Schneider et al., 2012), a semi-automatic, thresholdbased segmentation was carried out following the half-maximum
height method (HMH; Spoor et al., 1993) and the region of interest thresholding protocol (ROI-Tb; Fajardo et al., 2002) taking
repeated measurements on different slices of the virtual stack
(Coleman and Colbert, 2007).
Besides the pulp chamber volume of the incisors, 14 linear,
surface, and volumetric variables describing internal structural
variation and tissue proportions were digitally measured (or
derived) on MA 93 (Table 2). Intra- and inter-observer tests for
measurement accuracy run by two observers revealed differences
less than 4%, which is similar to previous analyses (e.g., Macchiarelli
et al., 2008; Bondioli et al., 2010; Zanolli et al., 2012).
Observations on the pulp cavity of the two incisors from Uadi
Aalad were compared with similar evidence from H. heidelbergensis
from Tighenif (isolated lower I1; Zanolli, 2011; Zanolli and
Mazurier, 2013), Neanderthals (Ehringsdorf G3 [upper I2] and
Regourdou 1 [lower I1]; Macchiarelli et al., 2013; NESPOS Database,
2013); and recent humans (original data).
To assess site-specific variation in their radicular dentine
thickness, ad hoc imaging techniques were used to virtually unroll the roots of the two incisors (15e85% portion of the total root
length) and to generate their morphometric maps (Bayle, 2008;
Bondioli et al., 2010; Bayle et al., 2011; Macchiarelli et al.,
2013). For comparative purposes, we also considered the
following specimens: the upper I2 Javanese H. erectus specimen
MI92.2 (HEJ: Zanolli, 2011); the North African H. heidelbergensis
isolated lower I1 from Tighenif (HHNA: Zanolli, 2011; Zanolli and
Mazurier, 2013); the two Neanderthal specimens Ehringsdorf G3
(upper I2) and Regourdou 1 (lower I1) (NEA: Macchiarelli et al.,
2013; NESPOS Database, 2013); and two recent human incisors
(EH: original data).
In all three Eritrean specimens, enamel thickness topographic
distribution was rendered through a 3D map generated using a
chromatic scale where thickness increases from thin (dark blue) to
thick (red) (Macchiarelli et al., 2008, 2013; Bayle et al., 2011). For
comparative purposes, similar cartographies have been generated
for a selected number of specimens representing H. erectus from
Sangiran (MI92.2 [upper I2] and NG0802.3 [lower M2]; Zanolli,
2011, 2013); North African H. heidelbergensis (isolated lower I1
and Tighenif 2 [lower M1 and M2]; Zanolli, 2011; Zanolli and
Mazurier, 2013); Neanderthals (Krapina D122 [upper I2], Regourdou 1 [lower I1], La Chaise de Vouthon S5 [lower M1], Krapina D10
[lower M2]; Macchiarelli et al., 2013; NESPOS Database, 2013); and
recent humans of European origin (original data).
The results of the 2e3D virtual analyses performed on MA 93
were variably compared with a number of fossil and recent samples
(Table 3).
Nonmetric features revealed by virtual imaging at the EDJ of MA
93 were scored according to Skinner et al. (2008a) for the accessory
cusps, Bailey et al. (2011) and Martínez de Pinillos et al. (2014) for
the trigonid crest pattern (see also Macchiarelli et al., 2006), and
Martinón-Torres et al. (2014) for the talonid crest expression.
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C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Table 3
Fossil and recent comparative samples used for assessing 2e3D molar crown tissue proportions.
Specimens/samples
References
H. habilis-rudolfensis from East Africa (HHR)
South African early Homo (SAEH)
Javanese H. erectus (HEJ)
North African H. heidelbergensis from Tighenif (HHNA)
Neanderthals (NEA)
Smith et al., 2012
Smith et al., 2012
Zanolli, 2011
Zanolli, 2011; Zanolli and Mazurier, 2013
Olejniczak et al., 2008a; Kupczik and Hublin, 2010;
Smith et al., 2012; Macchiarelli et al., 2013; NESPOS Database, 2013
Kupczik and Hublin, 2010
Smith et al., 2012
North African Aterians (AFMH)
African-Near Eastern anatomically modern fossil humans
(ANEFMH) from Morocco (Dar es-Soltane, Grotte des
Contrebandiers, Jebel Irhoud), South Africa (Die Kelders
Cave, Equus Cave) and Israel (Qafzeh)
The European early Upper Paleolithic specimen
from Lagar Velho (EUPH)
Recent humans (RH)
Bayle et al., 2010
Olejniczak et al., 2008a; Smith et al., 2012; original data
Geometric morphometric analyses
Comparative geometric morphometric analyses of the MA 93
EDJ were performed on the unsmoothed reconstructed virtual
surfaces by placing a total of seven landmarks on the apex of the
protoconid, metaconid, entoconid and hypoconid, and at each
intermediate lowest point between two dentine horns along the
dentine marginal ridge, except between the two distal horns (see
Zanolli et al., 2012). Because of the variable presence of the
hypoconulid, this latter cusp and the distal marginal ridge were
not considered (Zanolli and Mazurier, 2013). By using the package
Morpho 0.24.1 (Schlager, 2013) for R v.3.0.1 (R Development Core
Team, 2013), we performed a generalized Procrustes analysis
(GPA) and a between-group principal component analysis
(bgPCA) based on the Procrustes shape coordinates (Mitteroecker
and Bookstein, 2011). For the specific purposes of this analysis,
MA 93 was compared with a number of fossil and recent samples
(Table 4).
Results
Description of the specimens
UA 222 (Uadi Aalad) This upper left lateral permanent incisor
(ULI2) from an adult individual is complete from crown to root
(Fig. 1A). Macroscopically, there is some evidence of weathering,
root etching and sediment scratching. From the mCT record, it also
appears that the pulp cavity is filled with homogeneous finegrained sediment. The tooth shows advanced occlusal wear (stage
4), with functional enamel loss and extensive emerging dentine
creating a slightly labiolingual to mesiodistal oriented bevel.
Interproximal wear is more marked distally, where the
facet almost reaches the CEJ. While the occlusal surface is
smooth, with rare pits and few microstriations, SEM analysis of
its labial and, to a minor extent, lingual crown aspects revealed a
number of fine striations covering the entire surfaces. The
scratches, which can be interpreted as microwear traces (cf.
Ungar et al., 2008; Krueger and Ungar, 2010), are mostly vertical
or slightly oblique (85e90 range), sub-parallel and very thin (2e
3 mm) (Fig. 2A). However, some larger furrows show the
characteristics of trampling damage, with broad entry,
rectangular section, and narrow end (Fiore et al., 2004).
The uncorrected maximum MD crown diameter is 6.7 mm,
while the BL diameter is 7.2 mm (contra Macchiarelli et al., 2004a;
see Table 5). The root, which is complete with a closed apex displaying a thin cementum deposit on virtual sections, exhibits longitudinal grooves, the distal one being deeper. From the lowest
enamel cervical point to its apex, root length is 18.8 mm.
The enamel shows no evidence of linear enamel hypoplasia,
hypocalcifications or macro-defects, and no calculus or pathological lesions are noticeable. While part of its crown has been
removed by extensive wear, based on the preserved enamel UA 222
lacks shovelling (grade 0e1), an interruption groove and a distinct
tuberculum dentale, but does show labial convexity (Fig. 1A) and
also possesses a longitudinal lingual groove that is slightly deviated
mesially (cf. Martinón-Torres et al., 2012), reaching the wavy rim of
the preserved occlusal-lingual margin.
Microtomographic-based virtual sections reveal relatively thin
enamel (maximum 0.66 mm). The EDJ perfectly mirrors the outer
morphology. Despite a slight collar constriction from its occlusal
aspect to mid-root level, the pulp cavity shows a slightly labiolingually compressed ovoid outline. Conversely, its apical portion is
mesiodistally flattened, with marked labiolingual expansion
(Fig. 3A). Its total volume is 30.7 mm3. The standardized morphometric map of its virtually unrolled root reveals an area of absolutely thicker dentine (maximum 3.3 mm) on the labial aspect near
the cervix, while thinner dentine is deposited on two vertical strips
running along the mesial and distal aspects (Fig. 4A).
Table 4
Fossil and recent comparative samples used for in the geometric morphometric analyses of the molar EDJ.
Samples
Sites
a
Javanese H. erectus
North African H. heidelbergensisa
Neanderthals
Sangiran
Tighenif
Krapina
La Chaise-de-Vouthon
Regourdou
Ehringsdorf
Recent humans
a
Added a posteriori in the bgPCA analysis.
Lower M1
KRD77, KRD79, KRD80,
KRD81, KRD105
S5, S14e7, S49, BDJ4C9
Lower M2
References
NG0802.3
Tighenif 2
KRD1, KRD6, KRD10,
KRD86, KRD104, KRD107
Zanolli, 2011
Zanolli and Mazurier, 2013
NESPOS Database, 2013
Regourdou 1
Ehringsdorf I
14
17
Original data
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
101
Figure 1. The upper left I2 UA 222 (A) and the lower left I1 UA 369 (B) from Uadi Aalad, and the lower left M1/M2 MA 93 from Mulhuli-Amo (C). For each specimen, the images
show: the original (in lingual and mesial views for UA 222 and UA 369, in occlusal and buccal views for MA 93); a mesiodistal (left) and a labiolingual (right) virtual section for UA
222 and UA 369, and two virtual sections for MA 93 respectively passing through the mesial (upper) and the buccal cusps (lower); the microtomographic-based reconstruction of
(from the left): the outer surface (the enamel in red), the dentine (yellow), the occlusal view (for the two incisors) and, uniquely for MA 93, the pulp cavity (cyan) (same views as the
originals). b, buccal; l, lingual; m, mesial; o, occlusal. Scale bars, 1 cm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of
this article.)
UA 369 (Uadi Aalad) This specimen represents a complete lower
left central incisor (LLI1) from an adult. Serial virtual slices reveal a
pulp chamber filled almost completely by a matrix, which occasionally causes contrast attenuation with the dentine (Fig. 1B). UA
369 also exhibits advanced occlusal wear (stage 4; Smith, 1984),
with a major mesiodistal to labiolingual orientation resulting in a
weakly concave occlusal surface whose enamel rim is thicker
labially (0.9 mm versus 0.4 mm lingually). Interproximal wear is
more marked mesially. Under the stereomicroscope, the occlusal
surface is smooth, with rare pits and few microstriations. The
SEM imaging shows a microwear pattern similar to that seen in
UA 222 (Fig. 2B). Indeed, mastication-related pits and scratches,
as well as sediment-induced striae and furrows, are present on
both labial and lingual crown aspects, the former having
undergone some etching-like process that obscures part of the
features, particularly near the occlusal border. The majority of the
vertical, sub-parallel and thin striae (2e3 mm) correspond to
microwear traces (Teaford, 2007; Ungar et al., 2008; Hlusko et al.,
2013), while few longer (1e2 mm), slightly thicker (3e10 mm)
and randomly oblique scratches more likely result from the
abrasive action of variably sized sediment particles. Labially, close
to the CEJ, there are four long and relatively deep furrows of
taphonomic origin, with smooth walls and rounded bottom.
Although the general microfeature pattern does not differ from
UA 222, some of the scratches occurring on both faces indicate
that UA 369 may have experienced slightly different taphonomic
micro-dynamics.
The uncorrected maximum mesiodistal diameter corresponds
to 5.2 mm and the labiolingual diameter to 6.7 mm (Table 5).
Similar to UA 222, no linear enamel hypoplasia, hypocalcifications,
macro-defects, calculus deposits or pathological lesions are
noticeable on this specimen, and the preserved portion of the
crown shows no developed relief on its lingual and labial aspects, or
shovelling.
Measured on virtual sections, maximum enamel radial thickness reaches 0.8 mm. Internally, the dentine crown surface casts
the outer morphology. Also in this lower incisor the upper portion
of the pulp cavity, whose total volume corresponds to 15.9 mm3,
shows a labiolingually compressed ovoid outline, followed by a
marked mid-root labiolingual expansion and a mesiodistally flattened apical root morphology (Fig. 3B).
Well-developed longitudinal grooves run along both the mesial
and distal radicular aspects, whose maximum length reaches
16.3 mm. As revealed by its profile (Fig. 4B), thicker root dentine in
this lower incisor appears on the cervical half of the labial and
lingual aspects (maximum 2.9 mm), while the thinnest values are
found along the apical third of the mesial and distal faces.
For magnetic resonance microimaging-based growth assessment, a total of 20 consecutive measurements were possible on
both lingual and buccal aspects of the root in UA 369 (Fig. 5A), but
additional measurements became too difficult close to the root
apex beyond 12.5 mm on the buccal aspect, and 13.5 mm on the
lingual aspect of the root. The overall mean buccal extension rate
(n ¼ 20 estimates) was 8.0 mm per day (range 3.0e10.8 mm per day)
102
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Figure 2. SEM micrographs of the labial aspect of UA 222 (A) and UA 369 (B). Mostly
vertically-oriented thin microfeatures are visible on the central portion of the UA 222
crown (A), where the two larger and deeper furrows crossing near the centre of the
image result from sediment abrasion. Numerous thin microfeatures are also present on
the centre-mesial area spot sampling the UA 369 crown (B), together with few oblique
sediment traces and an etching damage on the upper right corner of the image. Scale
bars, 100 mm.
and the mean lingual extension rate was 7.8 mm per day (range 4.9e
10.0 mm per day). In both roots there was an early peak in root
extension rate (10.0 and 10.8 mm per day, respectively) between
1.32 and 1.48 years post enamel completion.
These results (Fig. 5B) are presented first as cumulative plots of
increasing lingual and buccal root length against root formation
time compared with data for a sample of 44 modern human incisor
tooth roots taken from Dean and Cole (2013). A second plot (Fig. 5C)
puts root growth into context with crown growth for illustrative
purposes. Root formation in UA 369 was compared with data for
crown growth in the same modern human sample (Dean and Cole,
2013). It was assumed that the unworn crown height in UA 369
would have been close to that of other unworn lower incisors
attributed to H. erectus s.l., a good example of which is the lower
central incisor of KNM-WT 15000 that measures 9.75 mm. Using
this tooth to provide an estimate of the crown formation time in UA
369 suggests that it would have taken close to 2.83 years to complete crown formation based on a nine day periodicity between
adjacent long-period striae of Retzius in the enamel of the Eritrean
specimen (Dean et al., 2001: Table 1). These estimates of crown
height and crown formation time allow the plots for UA 369 to be
visualized alongside the modern human sample and show that
there is little effect (compared with Fig 5B) on how rates of root
formation fall within the modern sample. Both plots (Fig. 5B and C)
show that root formation in UA 369 could be reconstructed over
approximately five years.
MA 93 (Mulhuli-Amo) This is a nearly unworn lower left first or
second permanent molar crown (LLM1/M2) of a juvenile individual
(Fig. 1C). The buccal and lingual surfaces are slightly etched from
roots and sediment, resulting in a coarse enamel texture. On the
distolingual surface, a shiny area of better preserved enamel
mimics an interproximal facet, but its lingually displaced position
and its broad extension (larger than the mesial interproximal
facet) support a taphonomic, non-functional origin. While some
shallow furrows are visible on the lingual aspect, the presence of
linear enamel hypoplasia cannot be confirmed here. Conversely,
some hints of widely spaced perikymata are still visible in the
centre of the distal face, where the enamel remains least worn. In
this position, there is indeed a weak expression of enamel
hypoplasia, supporting a similar conclusion for the lingual aspect.
The hypoplasia would have occurred during crown formation.
The rather squat crown reaches 6.1 mm in height at the metaconid and 6.2 mm at the protoconid. It shows a rectangular outline
with a length (MD) of 13.9 mm and a breadth (BL) of 11.9 mm
(Table 5). A slightly polished wear facet on the protoconid and two
smaller facets on the entoconid and on the hypoconulid indicate
that the tooth had begun functional occlusion, but in the earliest
stage (stage 1). A small, flat and ovoid interproximal mesial contact
facet (2.9 2.3 mm) is present, but there is no distal facet. The
mesial wall converges cervically, while the opposite is true buccally,
the lingual and distal walls being relatively vertical. The subhorizontal cervico-enamel line is almost completely preserved
and the fracture plane in the inferior part appears to follow the
incremental mineralizing front, which suggests that the tooth was
at the crown complete stage of formation.
There are five main cusps, including a medium-large hypoconulid (C5; stage 4), plus a small tuberculum intermedium (C7;
stage 2), but no tuberculum sextum (C6). Relative cusp size is
protoconid > metaconid > hypoconid > entoconid > C5 > C7. The
occlusal grooves connect in a þ fissure pattern. Compared with the
incised distal marginal ridge, the mesial margin is not crossed by
the central groove and is proportionally thicker and higher, forming
a deep elongated mesial fovea (stage 3). Immediately behind the
fovea, an uninterrupted sharp mid-trigonid crest (score 1A) links
the two mesial cusps. Two distal crests depart from the protoconid
and the metaconid, respectively. They converge in the trigonid
basin, but are interrupted in the centre by the main groove. Because
they do not connect, the latter can be interpreted as an incomplete
distal crest. Between the mid-trigonid crest and the distal trigonidlike feature, a short crest originating from the metaconid angles
towards the occlusal basin. No expression of a deflecting wrinkle is
found. The protostylid is absent and the intercuspal groove is
relatively shallow.
At the EDJ level, MA 93 exhibits a modestly elevated topography,
with relatively low but sharp dentine horns systematically underlying the blunter outer cusps, even at the level of the metaconulidtype C7 (Skinner et al., 2008a), which is located on the distal
shoulder of the metaconid dentine horn and is slightly better
expressed than at the outer surface. While on the occlusal surface
the mid-trigonid crest is complete but slightly dipping at the
sagittal sulcus level, its EDJ expression is continuous and of regular
height (grade 3; Bailey et al., 2011), originating slightly mesial from
the metaconid dentine horn and joining the protoconid dentine
middle lobe segment (middle-mesial configuration). Together with
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
103
Table 5
Crown dimensions (MD and BL diameters, in mm) of the two permanent incisors from Uadi Aalad (UA 222 and 369) and the permanent molar from Mulhuli-Amo (MA 93)
compared with some Pleistocene and recent human specimens/samples.
Specimens/samples
UA 222
UA 369
MA 93
HHR
HEA
HEG
HEJ
HEC
HA
HHNA
HHE
NEA
NEEHS
EUPH
RH
UI2
LI1
BL
BL
MD
LM1
BL
MD
LM2
BL
6.8
6.6e7.0
2
6.6
6.3e6.8
2
6.7
6.0e7.3
4
6.2
5.8e6.5
2
6.4 0.4
5.8e6.8
7
7.6
1
6.6
e
1
6.5 0.3
5.9e7.2
29
7.6 0.4
6.9e8.2
14
7.0
6.6e7.3
3
6.3 0.4
5.5e7.1
20
6.1 0.4
4.6e6.9
71
13.9
14.1 0.9
12.8e15.2
19
12.8 0.7
11.9e14.2
8
13.3
13.0e13.9
5
12.8 0.9
11.2e14.8
14
12.6 1.1
9.9e14.1
12
12.2
1
13.2
12.3e14.0
3
11.2 0.3
10.3e12.2
41
11.9 0.9
10.8e13.6
22
11.4
10.7e12.0
5
11.6 0.9
10.0e13.0
26
11.3 0.7
9.7e12.9
116
11.9
12.2 0.9
10.6e13.2
20
11.3 0.9
10.6e12.8
8
11.8
11.2e12.6
5
12.2 0.8
10.8e14.2
14
11.9 0.9
10.1e12.8
12
11.8
1
12.7
12.5e13.0
3
10.4 0.5
9.5e11.6
40
11.2 0.7
9.7e12.9
22
11.7
11.3e12.4
5
11.0 0.6
10.0e12.0
27
11.0 0.5
9.2e12.5
118
13.9
15.2 1.2
14.0e18.3
18
13.4 0.9
12.2e15.2
8
13.0
12.3e14.2
5
12.4 1.4
10.1e13.8
15
12.3 0.5
11.3e13.1
8
13.5
1
13.1
12.3e14.0
3
11.0 0.2
9.4e12.2
41
12.2 0.9
10.5e14.0
25
11.4
10.7e12.0
5
11.3 1.0
9.5e12.8
22
10.7 0.7
9.3e12.3
103
11.9
13.5 1.0
11.7e15.1
18
12.1 0.7
11.4e13.1
8
11.5
10.7e13.1
5
11.6 1.3
9.5e13.2
15
11.8 0.5
11.1e12.7
8
12.0
1
13.0
12.2e13.5
3
10.2 0.7
8.4e11.5
41
11.3 0.7
9.8e12.5
25
11.7
11.3e12.4
5
10.8 0.8
9.8e12.0
22
10.7 0.6
8.8e11.8
103
a
7.2
6.7
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
Mean
Range
n
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
Mean
n
Mean
Range
n
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
Mean (s.d.)
Range
n
6.6
6.0e7.9
4
8.3
8.2e8.5
3
6.9
e
1
7.3
7.0e7.7
3
8.1
8.0e8.2
3
8.2
1
8.5
e
1
7.7 0.3
7.3e8.3
27
8.7 0.6
7.8e9.9
22
7.7 0.5
7.0e8.1
7
6.8 0.5
6.0e7.4
10
6.5 0.5
5.4e7.2
61
a
A misprint occurred in the first description of the incisor UA 222 (Macchiarelli et al., 2004a: Table 1) and the correct value is reported here. The standard deviation (s.d.) is
provided only for the samples with n 7. EUPH: European early Upper Paleolithic humans (Frayer, 1977 [upper I2 and lower Ms]; Hillson et al., 2010 [lower I1]); HA:
H. antecessor from Atapuerca Gran Dolina (Bermúdez de Castro et al., 1999); HEA: African H. erectus/ergaster from Kenya and Ethiopia (Wood, 1991 [upper I2 and lower Ms];
Stynder et al., 2001 [lower I1]; Suwa et al., 2007 [lower Ms]); HEC: H. erectus from China (Wood, 1991); HEG: H. erectus from Georgia (Martinón-Torres et al., 2008 [lower I1,
upper I2 and lower Ms]; Lordkipanidze et al., 2013 [lower Ms]); HEJ: H. erectus from Java (Wood, 1991 [lower Ms]; Widianto, 1993 [lower Ms]; Grine and Franzen, 1994 [upper
I2]; Stynder et al., 2001 [lower I1]; Kaifu et al., 2005 [lower Ms]; Zanolli, 2013 [upper I2 and lower Ms]); HHE: European H. heidelbergensis from Atapuerca Sima de los Huesos
(Martinón-Torres et al., 2012); HHNA: North African H. heidelbergensis from Tighenif and Rabat (Wood, 1991 [lower Ms]; Stynder et al., 2001 [lower I1]; Martinón-Torres et al.,
2008 [upper I2]); HHR: H. habilis-rudolfensis from East Africa (Wood, 1991 [upper I2 and lower Ms]; Stynder et al., 2001 [lower I1]; Leakey et al., 2012 [lower Ms]); MA 93:
Mulhuli-Amo; NEA: Neanderthals (Voisin et al., 2012); NEEHS: Near Eastern early H. sapiens from Qafzeh (Vandermeersch, 1981); RH: recent humans (Frayer, 1977).
the small accessory ridge originating from the metaconid, the two
enamel distal crests departing from the protoconid and the metaconid and converging towards the centre of the trigonid basin
without joining each other are sharply expressed at the EDJ level.
This trigonid crest pattern is similar to the type 10 pattern recently
defined by Martínez de Pinillos et al. (2014). A 4-like type talonid
crest is also visible, but it slightly differs from the original classification of this trait provided by Martinón-Torres et al. (2014), as it
displays only a distal buccal segment of the trigonid crest shifting
distally towards the centre of the occlusal basin, along with the
expression of two short mesial and distal crest segments running
down from the entoconid and hypoconid dentine horns. In addition, a faint, short accessory ridge set mesially to the entoconid
obliquely runs from the marginal ridge towards the central basin
(cf. Martinón-Torres et al., 2014). However, while at the outer surface the anterior fovea is restricted to a buccolingual groove, a large
depression occupies the mesial quarter of the corresponding EDJ
occlusal basin (Fig. 1C). In inferior view, MA 93 exhibits a well
restricted, mature pulp chamber and thick broken dentine walls. At
the pulp cavity roof level, while the five main cusps are well represented and show that the roof formation was completed (Fig. 1C),
there is no relief corresponding to the C7 and to the crests running
in the occlusal basin.
Comparative analyses and discussion
UA 222 (ULI2) and UA 369 (LLI1)
External morphology Compared with the most common condition
characterizing the African and Eurasian Early-Middle Pleistocene
dental record (Wood, 1991; Brown and Walker, 1993; Grine and
Franzen, 1994; Bermúdez de Castro et al., 1999; Martinón-Torres
et al., 2007, 2008, 2012; Bailey and Hublin, 2013; Liu et al., 2013),
including eastern African specimens such as KNM-ER 808 and
KNM-WT 15000 (Wood, 1991; Brown and Walker, 1993), the
preserved crowns of both Eritrean incisors are featureless. Only
UA 222 displays a longitudinal lingual groove and a degree of
labial convexity comparable with that seen in some upper
104
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Figure 3. Virtual rendering of the pulp cavity of UA 222 (A) and UA 369 (B). UA 222 is compared with the Neanderthal upper I2 Ehringsdorf G3 (NEA; NESPOS Database, 2013), while
UA 369 is compared with the lower I1s of H. heidelbergensis from Tighenif (HHNA; Zanolli and Mazurier, 2013) and the Neanderthal Regourdou 1 (NEA; Macchiarelli et al., 2013). The
morphology virtually extracted from two recent human incisors (RH; original data) is also shown. d, distal; l, lingual; lb, labial; m, mesial. Scale bar, 5 mm.
incisors from Atapuerca Sima de los Huesos (e.g., the UI1s AT-165
and 554; Martinón-Torres et al., 2012). While advanced occlusal
wear has partially erased their original morphology, notably in
the case of UA 222, both specimens lack any trace of either
lingual finger-like extensions or a distinct basal eminence as seen
in some Eurasian later Middle Pleistocene upper incisors
(Hershkovitz et al., 2011; Martinón-Torres et al., 2012; Liu et al.,
2013). On the other hand, the lack of an interruption groove on
the maxillary incisor fits the figures reported for H. erectus s.l.
(Manni et al., 2007; see also; Bailey, 2006).
For their general outline and outer gross features, as well as for
the elongated root with two shallow but proportionally large longitudinal grooves, the incisors from Uadi Aalad globally resemble
the morphology displayed by the Early Pleistocene lower I2 from
’Ubeidiya, Israel (Belmaker et al., 2002). The Near Eastern specimen
(UB 335) shows relatively small crown size, lack of a lingual
tuberculum, probable absence of the mesial and distal marginal
ridges, and marked mesial and distal longitudinal root grooves
(Belmaker et al., 2002), a pattern which better fits the characteristics of the two incisors from Buia rather than those displayed by
KNM-WT 15000 (Brown and Walker, 1993).
For its buccolingual crown diameter, UA 222 closely approximates the estimates available for Javanese H. erectus (Grine and
Franzen, 1994; Zanolli, 2013) but, with the exception of Homo
habilis-rudolfensis from East Africa and Georgian H. erectus, this
tooth is systematically smaller compared with the Early-Middle
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
105
Figure 4. Standardized morphometric maps of the virtually unrolled tooth root (15e85% of the total root length) of UA 222 (A) and UA 369 (B). Dentine topographic variation is
rendered by a thickness-related chromatic scale increasing from dark blue (0) to red (1). UA 222 is compared with similar evidence from the H. erectus UI2 MI92.2 from Sangiran
(HEJ, represented only by the root portion closer to the cervix; Zanolli, 2011, 2013) and the Neanderthal specimen Ehringsdorf G3 (NEA; NESPOS Database, 2013), while UA 369 is
compared with the lower I1s of H. heidelbergensis from Tighenif (HHNA; Zanolli and Mazurier, 2013) and the Neanderthal Regourdou 1 (NEA; Macchiarelli et al., 2013). The maps
illustrating the condition of two recent human incisors (RH; original data) are also shown. d: distal; l: lingual; lb: labial; m: mesial. (For interpretation of the references to colour in
this figure legend, the reader is referred to the web version of this article.)
Pleistocene specimens/samples included in the present study
(notably, the African H. erectus/ergaster sample from eastern Africa;
Martinón-Torres et al., 2008), and only exceeds the European early
Upper Paleolithic and the recent human average values (Table 5).
For the same variable, the lower incisor UA 369 exceeds the estimates of the H. erectus samples from Java and China (Stynder et al.,
2001), but fits those of African and Georgian H. erectus (Stynder
et al., 2001; Martinón-Torres et al., 2008), H. habilis-rudolfensis
(Stynder et al., 2001), and both African and European samples
representing H. heidelbergensis, the highest BL values being displayed by Homo antecessor (Stynder et al., 2001; Martinón-Torres
et al., 2012) and Neanderthals (Table 5).
Crown microwear The microfeatures observed on the labial and
lingual crown aspects of both Eritrean incisors (Fig. 2) differ in their
morphology and lack of shallowness and orientation from the
typically labial scratches found on some Neanderthal and preNeanderthal incisors and canines, which have been referred to
nonalimentary/manipulative behaviours (Lozano et al., 2009;
Frayer et al., 2010, 2011; Volpato et al., 2012). These marks
represent either diet-related microstriations (Ungar et al., 2006;
Teaford, 2007) and/or are the result of taphonomic processes.
Nonetheless, besides the presence in both specimens of randomly
oriented scratches probably resulting from the abrasive action of
variably sized sediment particles, their labial surfaces reveal a
qualitatively and quantitatively similar microtextural pattern
consisting of thin (2e3 mm), sub-parallel, mostly vertical (or
slightly oblique) fine striations. While microwear analyses of PlioPleistocene hominins, including early Homo and H. erectus s.l.,
Figure 5. (A) UA 369 (lower left I1). mMRI labiolingual slice (pixel size, 58.6 mm; slice thickness, 200 mm) through the centre of the root. Scale bar, 500 mm. (B) Root length (in mm) is
plotted against root formation time (in years). The grey filled circles represent 44 modern human incisor roots. The blue filled circles represent the buccal and lingual plots for UA
369 calculated to be 80 days apart (2.5 mm per day over 200 mm of dentine formation). The red filled triangles represent the labial and lingual plots for UA 369 calculated to be 90
days apart (2.3 mm per day over 200 mm of dentine formation). All roots are plotted as if zero root height occurred at zero formation time. (C) Tooth length (cumulative crown and
root height in mm) for 44 modern human incisors (open black circles) is plotted against tooth formation time (in years). For some modern humans continuous data are available for
crown growth but for others the beginning of root growth is placed at the time of crown completion and the height of the crown at the end of enamel formation. The blue filled
circles represent the buccal and lingual plots for UA 369 calculated to be 80 days apart (2.5 mm per day over 200 mm of dentine formation). The red filled triangles represent the
labial and lingual plots for UA 369 calculated to be 90 days apart (2.3 mm per day over 200 mm of dentine formation). (For interpretation of the references to colour in this figure
legend, the reader is referred to the web version of this article.)
106
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Figure 6. Enamel thickness cartographies of UA 222 (A) and UA 369 (B), both in labial (lb) and lingual (l) views, and of MA 93 (C), in occlusal view. Topographic variation is rendered
by a tooth-specific thickness-related pseudo-colour scale ranging from thinner dark-blue to thicker red. Isolated white areas correspond to complete enamel removal following
occlusal wear. UA 222 is compared with similar evidence from the H. erectus upper I2 MI92.2 from Sangiran (HEJ; Zanolli, 2011, 2013) and the Neanderthal specimen Krapina D122
(NEA; NESPOS Database, 2013). UA 369 is compared with the lower I1s of H. heidelbergensis from Tighenif (HHNA; Zanolli and Mazurier, 2013) and the Neanderthal Regourdou 1
(NEA; Macchiarelli et al., 2013). MA 93 is compared with the lower M1s of H. heidelbergensis Tighenif 2 (HHNA; Zanolli and Mazurier, 2013) and the Neanderthal S5 from La Chaise
de Vouthon (NESPOS Database, 2013) and to the lower M2s of H. erectus NG0802.3 from Sangiran (Zanolli, 2011, 2013), H. heidelbergensis Tighenif 2 (HHNA; Zanolli and Mazurier,
2013) and the Neanderthal Krapina D10 (NESPOS Database, 2013). For each tooth type, the map illustrating the condition of a recent human tooth (RH; original data) is also shown.
Independently from their original side, all teeth are shown as left. Scale bar, 1 cm. (For interpretation of the references to colour in this figure legend, the reader is referred to the
web version of this article.)
have concentrated on cheek teeth (e.g., Ungar et al., 2006, 2012;
Pontzer et al., 2011; Ungar, 2011; Ungar and Sponheimer, 2011), it
has been suggested that there was a probable decrease in incisor
use in African H. erectus compared with H. habilis and Homo
rudolfensis, either because of a change in diet (broader spectrum;
Ungar and Sponheimer, 2011) and/or increased extraoral food
processing (Ungar, 2011). Accordingly, the evidence from the
Eritrean teeth better supports the model of an anisotropic surface
whose textural microfeatures indicate a moderate degree of
complexity resulting from the consumption of relatively soft and
tough foods, rather than that of an isotropic-like microwear
pattern made by a more complex blend of pits and striations
indicating the consumption of hard and brittle food (Ungar and
Sponheimer, 2011).
Root growth The results presented here demonstrate that high
resolution MRI micro-imaging clearly has the potential to enable
growth data to be retrieved non-destructively from fossil tooth
roots. Only a w5 year span of root growth could be reconstructed
in UA 369, as growth increments in the apical portion of the root
became indistinct. However, if the period between birth and the
initiation of incisor mineralization (w0.25 years), the crown
formation time (w2.83 years), and the missing apical formation
time were each added to the w5 year root formation time
documented here, the expectation is that the chronological age of
incisor root completion in UA 369 would have been
approximately eight to 10 years, as it is in modern humans. This
implies that longer roots in H. erectus s.l. might, at least partly, be
formed at the expense of slightly shorter crown formation times.
Alternatively, as in some great ape tooth roots, a second rise in
root extension rates in the apical portion of the root might also
have contributed to longer roots forming in approximately the
same time period as modern humans.
It has previously been suggested that apical closure of the
anterior teeth in African H. erectus (KNM-WT 15000) may have
occurred at similar chronological ages to modern humans (Dean,
2010) and the preliminary data from this study do not suggest
otherwise. The average rates of root growth in UA 369 also appear
to fall within those known for modern humans, although it remains
to be seen if the pattern and the timing of the root growth spurts
were similar or different in H. erectus s.l. The potential to gather
data for larger samples of fossil teeth non-destructively using this
technique now means questions such as this can be addressed.
Internal structure As revealed by the virtual cartographies illustrating enamel distribution in a selected number of tooth crowns
sampling Indonesian H. erectus, North African H. heidelbergensis,
Neanderthals and recent humans (Fig. 6A, B), UA 222 and UA 369
share a relatively thin enamel, notably on the lingual aspect.
However, while UA 222 apparently exhibits the thinnest labial
and lingual enamel in the comparative sample of fossil and recent
human upper permanent incisors available to us, UA 369 more
closely approximates the Neanderthal condition (Macchiarelli
et al., 2013).
The upper incisor UA 222 presents a peculiar pulp morphology
resulting in a slightly labiolingually compressed ovoid outline followed by a markedly mesiodistally flattened root canal, from the
crown ceiling to the mid-root level (Fig. 3A). In comparison, the
Neanderthal upper I2 from Ehringsdorf, for example, displays a
much higher volume (59.8 versus 30.7 mm3 in UA 222) and a
regularly-shaped ovoid cavity all along the root (Fig. 3A). While
morphologically closer to UA 222, the extant human data available
to us (mean volume 17.2 mm3) do not provide evidence of any
accentuated mid-root mesiodistal flattening.
The pulp cavity of UA 369 is similar to UA 222, but with an
accentuated mesiodistal flattening starting just below the crown
and involving the entire root portion, but notably its mid-region
(Fig. 3B). In this respect, UA 369 nears the morphology of the
Neanderthal specimen Regourdou 1 (volume 15.6 mm3;
Macchiarelli et al., 2013; see also Le Cabec et al., 2013), but also the
most common pattern displayed by the recent human lower incisors available in our sample (mean volume 11.0 mm3) (Fig. 3B). A
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
mesiodistally flattened radicular canal compatible with the outline
of the Eritrean lower incisor also characterizes the lower I2 specimen UB 355 from ’Ubeidiya (Belmaker et al., 2002) and the
recently reported Early Pleistocene lower I2 from Atapuerca Sima
del Elefante, Spain (Prado-Simón et al., 2012). Conversely, the early
Middle Pleistocene isolated lower I1 from Tighenif (volume
15.8 mm3) exhibits a spatula-like shape at crown level turning into
a regularly-shaped canal with an ovoid cross-section along the
entire radicular portion (Zanolli and Mazurier, 2013) (Fig. 3B).
Topographic variation in root dentine thickness of both Eritrean
incisors has been rendered through a morphometric map generated by virtually unzipping and then unrolling 15e85% of the total
root length (Fig. 4). Even if the significance (genetic versus functional) of the variation in root dentine thickness is not yet fully
understood (Bayle et al., 2012) and few specimens have been
detailed so far (Bayle, 2008; Bondioli et al., 2010; Bayle et al., 2011;
Macchiarelli et al., 2013), we note some differences among the
cartographies of the fossil and recent specimens considered in this
study. More specifically, while in UA 222 a unique thicker area is
found on the labial aspect near the CEJ, in the maps representing
Indonesian H. erectus, Neanderthals and recent humans, vertically
extended thicker dentine is present both labially and lingually.
Furthermore, at least in the Neanderthal and modern human roots,
the regions where absolutely and relatively thinner dentine is
found are much less spread and confined to the lower portion of the
map (Fig. 4A). Conversely, UA 369 root topography globally overlaps
the pattern of dentine thickness distribution expressed by the
North African H. heidelbergensis and Neanderthal representatives
used in this study, while the modern human cartography locally
shows relatively thinner dentine (Fig. 4B).
MA 93 (LLM1/M2)
External morphology The comparison between the occlusal
morphology of MA 93 and earlier East African lower molars sampling H. erectus/ergaster (e.g., KNM-ER 730, 820, 992, KNM-WT
15000), as well as with the geographically closer specimens from
Konso (Suwa et al., 2007) and Melka Kunture (Condemi, 2007;
Morgan et al., 2012) in Ethiopia, reveals a common general
pattern. However, while the presence of five main cusps
separated by a Y-shaped groove is found almost ubiquitously in
Early Pleistocene African lower M1s (Wood, 1991; Bermúdez de
Castro et al., 1999; Martinón-Torres et al., 2007, 2008), MA 93
shows a cusp organization resulting in a þ fissure pattern more
commonly found in the Early Pleistocene lower M2s (GómezRobles et al., 2014). While not very common in the African record,
the cruciform groove pattern is relatively frequent in Indonesian
H. erectus (Zanolli, 2013) and in Middle Pleistocene Eurasian
lower M2s and M3s (Bermúdez de Castro et al., 1999; MartinónTorres et al., 2007, 2012; Bailey and Hublin, 2013).
Cusp size sequence in MA 93, with a larger protoconid than the
metaconid and a medium-large hypoconulid, fits the average
pattern found in Early Pleistocene Afro-European lower M1s and
M2s (e.g., KNM-ER 820 and 992 (Wood, 1991), ATD6-5 (Bermúdez
de Castro et al., 1999)). In addition, MA 93 exhibits a welldeveloped and complete mid-trigonid crest, which even if found
in Georgian H. erectus and frequent in H. erectus s.s., is generally
absent or interrupted by the central groove in African H. erectus/
ergaster specimens like KNM-ER 820, 992 and KNM-WT 15000
(Wood, 1991; Brown and Walker, 1993; Martinón-Torres et al., 2007,
2008; Bailey and Hublin, 2013; Zanolli, 2013). Unlike most AfroEuropean H. erectus lower molars, like D211 (Martinón-Torres
et al., 2008), KGA10-1 (Suwa et al., 2007), KNM-ER 820 and KNMWT 15000 (Wood, 1991; Brown and Walker, 1993), the Eritrean
molar lacks any expression of a deflecting wrinkle, while the
107
presence of a C7, better expressed at the EDJ than at the outer
enamel surface, is compatible with the high frequency of this trait
observed in H. erectus (Manni et al., 2007; Bailey and Hublin, 2013).
Interestingly, in addition to its specific features, MA 93 closely resembles the LM1 KGA10-1 from Konso (Suwa et al., 2007), the two
sharing a rectangular occlusal outline, the presence of a C7, the lack
of protostylid (which is, conversely, quite a common feature in
H. erectus s.l.; Manni et al., 2007), and low and nearly parallel lateral
crown walls. To a lesser extent, the same is true for the lower M2 of
the same specimen, even if the latter shows a slight buccolingual
tapering of the talonid resulting into a more rounded occlusal
outline (Suwa et al., 2007).
Regardless of its serial position, MA 93 exhibits an absolutely
mesiodistally extended crown (Table 5). If MA 93 is an M2, its MD
dimension nears the averages of African H. erectus s.l. (Wood, 1991;
Suwa et al., 2007) and of the Dmanisi sample (Martinón-Torres
et al., 2008; Lordkipanidze et al., 2013), as well as the single value
available so far for H. antecessor (Bermúdez de Castro et al., 1999),
but exceeds those of all remaining Early to Middle Pleistocene
comparative samples except H. habilis-rudolfensis, the latter again
displaying the greatest anteroposterior crown diameter (Leakey
et al., 2012). Under this scenario, while the breadth of MA 93
does not deviate from the estimates of most among the samples
considered in this analysis (notably, from African, Georgian, Chinese, and Javanese H. erectus; Wood, 1991; Suwa et al., 2007;
Martinón-Torres et al., 2008; Lordkipanidze et al., 2013; Zanolli,
2013), it is lower than measured in H. habilis-rudolfensis and
North African H. heidelbergensis. The Eritrean molar also exceeds
estimates from European H. heidelbergensis (Table 5).
Internal structure Comparative tooth crown tissue proportions in
MA 93 and some fossil and recent human specimens/samples are
given in Table 6 (2D estimates) and Table 7 (3D). The comparative
record available for these kind of structural variables remains
quantitatively scanty in paleoanthropology and the extent of
intra-taxic/population variation is still virtually unknown, but
regardless of whether assigned to M1 or M2, the Eritrean
specimen exhibits rather low 2D values, notably for the enamel
area (c). However, for dentine area (b) and enamel-dentine
junction length (e), the specimen fits the estimates from two
South African early Homo M1s (Smith et al., 2012), and is also
near those from an isolated Javanese H. erectus M2 crown for the
variables c, e, and AET (Zanolli, 2011) (Table 6).
The number of comparative observations reported so far for 3D
inner tooth structural organization is even more limited, notably
for the LM1s (Table 7), the most investigated fossil humans being
the Neanderthals (Macchiarelli et al., 2006, 2007, 2008, 2013;
Olejniczak et al., 2008a; Kupczik and Hublin, 2010). However,
while for the enamel (Ve), dentine (Vcd), and pulp (Vcp) volumes
the Eritrean crown falls within the range of variation known for
Neanderthals and recent humans, as an M2 it differs from the figures expressed by the single representatives available to us of
Indonesian H. erectus (Zanolli, 2011) and H. heidelbergensis from
Tighenif (Zanolli and Mazurier, 2013), as well as from the later
North African Aterians (Kupczik and Hublin, 2010).
A different picture is provided by the comparison for the percent
ratio Vcdp/Vc, which represents the coronal portion that is dentine
and pulp, a directly comparable, size-independent parameter
rather finely describing internal crown structural organization. In
this case and specific comparative context, the structurally most
distant signature with respect to MA 93 is represented by the
virtually unworn H. erectus lower M2 from Java used in this study
(specimen NG0802.3; Zanolli, 2013). This specimen shows the
lowest ratio of any Pleistocene specimen reported so far and contrasts with the higher figures provided by our specimen sampling
108
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Table 6
2D-based linear and surface structural variables (crown tissue proportions) assessed
in MA 93 and compared with some Pleistocene and recent human specimens/
samples.
Specimens/
samples
c (mm2)
b (mm2)
e (mm2)
MA 93
Lower M1
HHR (1)
SAEH (2)
18.6
38.2
18.6
1.0
16.2
30.7
33.8
47.0
37.0
20.9
19.2
1.5
1.8
21.6
43.0
21.6
26.1
43.9
22.0
22.0
40.5
20.4
1.0
0.9e1.2
1.2
1.0e1.5
1.1
0.8e1.4
21.5
29.0
28.7e29.3
15.5
12.7e20.5
18.0
15.2e23.3
17.0
11.8e22.6
34.6
21.2
25.2
21.1
43.4
31.2
47.7
44.6
20.1
17.4
21.1
20.5
27.9
49.2
21.8
22.2
34.4
18.5
1.7
1.2
1.2
1.0
1.0e1.1
1.3
1.2e1.4
1.2
0.9e1.6
26.2
21.7
17.3
15.5
13.9e16.5
18.3
16.3e20.2
20.5
14.8e27.7
NEA (13)
ANEFMH (6)
RH (58)
Lower M2
HHR (1)
HEJ (1)
HHNA (1)
NEA (6)
ANEFMH (4)
RH (47)
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
Mean
Range
AET (mm)
RET
ANEFMH: pooled African-Near Eastern anatomically modern fossil humans from
Morocco, South Africa and Israel (Smith et al., 2012); HEJ: Javanese H. erectus from
Sangiran (Zanolli, 2011, 2013); HHNA: North African H. heidelbergensis from Tighenif (Zanolli and Mazurier, 2013); HHR: H. habilis-rudolfensis from East Africa (Smith
et al., 2012); NEA: Neanderthals (Smith et al., 2012); RH: recent humans (Smith
et al., 2012); SAEH: South African early Homo (Smith et al., 2012).
North African H. heidelbergensis and the typical Neanderthal
pattern (Olejniczak et al., 2008a) (Table 7).
Whether an M1 or M2, the crown from Mulhuli-Amo has
intermediate-thick enamel (Martin, 1985) with comparable 2e3D
AET and RET values (Tables 6 and 7) systematically below the estimates from any Early and Middle Pleistocene specimen/sample
known to us, notably African early Homo (Smith et al., 2012) and
Javanese H. erectus (Zanolli, 2011). To a lesser extent, enamel
thickness is below the values for early anatomically modern
humans from Africa (Smith et al., 2012) and Europe (Bayle et al.,
2010). The closest fits in our comparative analysis are an only
slightly thicker early Middle Pleistocene lower M2 from Tighenif
(Zanolli and Mazurier, 2013) and the Neanderthals (Olejniczak
et al., 2008a; Smith et al., 2012; Macchiarelli et al., 2013) (Fig. 6C).
Noteworthy, for enamel thickness MA 93 falls near the lower limits
of the modern human molar variation range.
At the EDJ, MA 93 exhibits some non-metric features similar to
the condition recently reported for the lower M1 of the early
Middle Pleistocene adult left hemi-mandible Tighenif 2, (Zanolli
and Mazurier, 2013), particularly the presence of a metaconulidtype C7 (while the lower M2 of the Algerian specimen displays
an interconulid-type C7). However, in the Eritrean molar the
complete mid-trigonid crest expresses a middle-mesial configuration of grade 3, absent in the North African fossil assemblage
sampling H. heidelbergensis but recorded with a relatively high
frequency in Neanderthals and, more rarely, in recent humans
(Bailey et al., 2011).
When compared to the condition revealed at the EDJ level by
some fossil human lower M1s and M2s (the proportionally higher
dentine horns and the rounder, more buccolingually extended
occlusal basin displayed by the H. erectus lower M2 from Sangiran;
Zanolli, 2011), MA 93 shows absolutely and relatively low dentine
horns (Fig. 7).
Geometric morphometric analyses
The results of the between-group principal component analysis
(bgPCA) based on the EDJ Procrustes shape coordinates of the lower
M2s of the MA 93 Eritrean specimen, of a Javanese H. erectus and of
a North African H. heidelbergensis, compared to structural evidence
from lower M1s and LM2s in two samples of Neanderthal (n ¼ 17)
and recent human (n ¼ 31), are shown in Fig. 8. The analysis of the
between-group principal component scores in reference to the
centroid size (Mitteroecker and Bookstein, 2011) suggests that
there is a weak allometric signal in the group separation, present
only for the bgPC1 (R2 ¼ 0.098). As expected, the bgPCA allows a
rather good discrimination between Neanderthals and recent
humans (along the bgPC1), as well as between lower M1s and M2s
(along the bgPC2). In this context, not only is MA 93 clearly set apart
from both comparative samples, but also from the two late Earlye
early Middle Pleistocene Javanese and Algerian specimens included
in the analysis.
A relatively low EDJ topography, a feature characterizing the
shapes on the extreme negative portion of the bgPC2 axis where
MA 93 is located (Fig. 8), is reminiscent of the ancestral hominin
Table 7
3D-based linear, surface, and volumetric structural variables (crown tissue proportions) assessed in MA 93 and compared with some Pleistocene and recent human specimens/
samples.
Ve (mm3)
MA 93
Lower M1
NEA (17)
EUPH (1)
RH (13)
Lower M2
HEJ (1)
HHNA (1)
NEA (11)
AFMH (3)
RH (26)
Vcd (mm3)
Vcp (mm3)
Vcdp (mm3)
Vc (mm3)
SEDJ (mm2)
Vcdp/Vc (%)
3D AET (mm)
261.4
316.8
15.4
332.2
593.5
256.1
56.0
1.0
14.7
3D RET
Mean
Range
Mean
Mean
Range
255.7
189.8e350.4
283.6
245.9
204.2e349.9
375.4
275.3e490.2
260.3
283.1
226.9e392.4
15.2
3.7e37.0
37.6
14.7
2.7e34.5
366.4
281.3e510.8
298.0
288.1
186.8e420.8
622.2
490.1e831.8
581.6
534.0
399.4e770.7
238.0
129.3e334.4
222.5
224.9
165.7e271.1
58.87
52.0e63.6
51.2
53.7
46.8e57.3
1.1
0.8e1.6
1.3
1.1
0.9e1.4
15.6
11.8e24.0
19.1
16.7
14.5e22.4
Mean
Mean
Mean
Range
Mean
Range
Mean
Range
240.8
373.1
276.0
169.1e397.4
343.0
306.7e371.2
237.2
136.4e361.9
217.2
480.2
353.2
242.2e493.7
399.0
351.1e469.1
238.0
167.9e396.5
1.9
22.3
13.7
1.5e28.2
8.4
3.6e17.1
13.6
0.8e35.5
219.2
502.4
366.9
250.0e519.3
407.4
354.7e486.2
249.5
135.3e426.0
460.0
875.5
642.6
436.1e895.7
760.3
665.0e859.2
486.7
306.6e770.0
181.1
312.5
252.3
182.5e345.6
265.9
236.7e304.1
195.7
95.4e285.4
47.7
57.4
57.1
51.0e64.2
53.4
50.4e56.6
51.0
42.7e57.3
1.3
1.2
1.1
0.8e1.3
1.3
1.2e1.4
1.3
0.7e2.3
22.1
15.0
15.4
11.9e20.9
17.6
14.7e19.9
20.2
12.6e40.7
AFMH: North African Aterians (Kupczik and Hublin, 2010); EUPH: the European early Upper Paleolithic human from Lagar Velho (Bayle et al., 2010); HEJ: Javanese H. erectus
from Sangiran (Zanolli, 2011, 2013); HHNA: North African H. heidelbergensis from Tighenif (Zanolli and Mazurier, 2013); NEA: Neanderthals (Olejniczak et al., 2008a; Kupczik
and Hublin, 2010; Macchiarelli et al., 2013; NESPOS Database, 2013); RH: recent humans (Olejniczak et al., 2008a; and original data).
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
109
Figure 7. Virtual rendering of MA 93 in occlusal and buccal views (A). Following each projection, it is shown (from the left) the outer crown (red), the dentine (gold) with the
enamel in semi-transparency (grey), and the distinct topography of the EDJ (yellow). In (B), MA 93 is compared with the lower M1s of H. heidelbergensis Tighenif 2 (HHNA; Zanolli
and Mazurier, 2013), the Neanderthal S5 from La Chaise de Vouthon (NEA; NESPOS, 2013) and the European early Upper Paleolithic Lagar Velho 1 (EUPH; Bayle et al., 2010), and in
(C) with the lower M2s of H. erectus NG0802.3 from Sangiran (Zanolli, 2011, 2013), H. heidelbergensis Tighenif 2 (HHNA; Zanolli and Mazurier, 2013) and the Neanderthal Regourdou
1 (Macchiarelli et al., 2013). The maps illustrating the condition of a recent human lower M1 and M2 (RH; original data) are also shown. Independently from their original side, all
crowns are shown as left. Scale bar, 1 cm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
condition (Macchiarelli et al., 2004b; Skinner et al., 2008a,b;
Olejniczak et al., 2008b; Braga et al., 2010). However, as revealed
by histological or virtual sections of some specimens from East
Africa (Beynon and Wood, 1986), H. antecessor from Gran Dolina
(Bermúdez de Castro et al., 2010) and Asian H. erectus (Dean et al.,
2001; Smith et al., 2009), low dentine horns are rather common in
Early and Middle Pleistocene Homo compared with the more
elevated and sharper derived morphology commonly seen in Late
Pleistocene and recent humans (Olejniczak et al., 2008a; Skinner
et al., 2008a, 2010). Nonetheless, besides the Eritrean specimen,
the condition typical of Early Pleistocene African Homo, if any, is
still unreported in a 3D perspective.
Concluding remarks
The discovery of ca. 1 Ma human remains in the area of Buia,
Danakil Depression of Eritrea, provides new insights about the
variation, geographic extent and evolutionary trends in
H. erectus/ergaster near the end of the Early Pleistocene, a period
still poorly sampled in the East African fossil record (Gilbert and
Asfaw, 2008). The geographic setting of the Dandiero Rift Basin
suggests the region may have recurrently played the role of a
buffer zone in human dispersal towards North Africa and the
Near East during various phases of the Pleistocene (Abbate and
Sagri, 2012).
110
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
Figure 8. Between-group principal component analysis (bgPCA) of the Procrustes
shape coordinates of the EDJs of MA 93 and the LM2 specimens NG0802 representing
H. erectus from Sangiran (HEJ; Zanolli, 2011, 2013) and Tighenif 2 sampling North African H. heidelbergensis (HHNA; Zanolli and Mazurier, 2013) compared with two lower
M1 and lower M2 samples consisting of 17 Neanderthals (NEA) and 31 recent humans
(RH), respectively. See the text for details on the composition of the Neanderthal and
recent human samples. The size of the circles is directly correlated with the centroid
size.
Compared with the condition more typical of African and
Eurasian Early and Middle Pleistocene anterior teeth (e.g., Wood,
1991; Manni et al., 2007; Martinón-Torres et al., 2007, 2012;
Bailey and Hublin, 2013; Bermúdez de Castro and MartinónTorres, 2013), while occlusally worn, the incisors from Uadi Aalad
apparently lack any developed expression of accessory features
(i.e., distinct tubercles, ridges, or cusp-like features expressed in the
cingular region of the lingual surface). For its buccolingual crown
diameter, the lower central incisor UA 369 falls within the range of
variation of most Early and Middle Pleistocene samples, while the
upper lateral incisor is relatively small compared with early African
Homo, but still comparable with the Javanese H. erectus estimates
(Zanolli, 2013). Enamel thickness variation is no longer considered
a useful trait to assess intertaxic evolutionary relationships (Smith
et al., 2012). Nonetheless, it is noteworthy that the Eritrean incisors
share relatively thin enamel, absolutely thinner than measured in
the early Middle Pleistocene North African assemblage of Tighenif
(Zanolli and Mazurier, 2013). They also show a topographic pattern
on the labial aspect closer to Neanderthals than to the modern
human condition. In this respect, it would be interesting to
compare the Eritrean specimens to the structural signature virtually extracted from the lower I2s of ’Ubeidiya (Belmaker et al., 2002)
and the ca. 1.3 Ma old ATE9-1 partial mandible of Sima del Elefante,
Spain (Carbonell et al., 2008; Bermúdez de Castro et al., 2011). The
latter shares with UA 369 some morphological details of the
radicular canal (Prado-Simón et al., 2012). Conversely, additional
methodological research is needed before appropriately interpreting the differences in radicular dentine thickness distribution,
even if the fossil specimens detailed in this study share a pattern
characterized by more accentuated contrasts (notably, near the CEJ)
than recorded in modern human anterior teeth (cf. Bayle et al.,
2011, 2012).
Together with the lack of a deflecting wrinkle and protostylid, a
peculiar feature on the outer occlusal surface of the lower M1/M2
MA 93 crown from Mulhuli-Amo is a cruciform fissure. While
observed at Dmanisi (Martinón-Torres et al., 2008) and also present
in Indonesian H. erectus (Martinón-Torres et al., 2008; Zanolli,
2013), this pattern is more common in Middle Pleistocene
mandibular molars (Martinón-Torres et al., 2007; Gómez-Robles
et al., 2014). However, it should be noted that, at least for the late
Early and Middle Pleistocene African fossil record, the time-related
variation patterns in morphological dental trait distribution have
not yet undergone the scrutiny of theoretical evolutionary models,
such as ‘random walk’ (i.e., Brownian motion) type (Hunt, 2007;
see; Gómez-Robles et al., 2014).
Dimensionally, the Eritrean molar has a mesiodistal diameter
of 13.9 mm, intermediate between the lower M1 (13.5 mm) and
the lower M2 (14.4 mm) of the KGA10-1 partial mandible from
Konso, Ethiopia (Suwa et al., 2007). Conversely, its buccolingual
diameter is small compared with the same teeth (11.9 mm versus
12.8 and 13.0 mm, respectively). Its mesiodistal size contrasts
with the short postcanine maxillary tooth row displayed by the
UA 31 cranium from the nearby, quasi-contemporaneous site of
Uadi Aalad. This maxilla has buccolingually, not mesiodistally,
expanded molar sockets (Abbate et al., 1998; Macchiarelli et al.,
2004a) and its proportions would better fit a shorter mandibular dental arcade than seen in other H. erectus/ergaster African
specimens (e.g., Wood, 1991; Brown and Walker, 1993; Suwa et al.,
2007; Wood and Leakey, 2011). Given the striking morphological
similarity between UA 31 and the newly discovered (but still
unreported) cranial remains from Mulhuli Amo (Coppa et al.,
2014), the extent of anteroposterior crown development displayed by MA 93 suggests a certain degree of (likely sex-related)
dentognathic structural variation in Africa around 1 Ma. In this
regard, it is also interesting to note that the virtually contemporaneous upper M1 specimen COR 2011 from Cornelia-Uitzoek,
South Africa, shows a large MD diameter (13.8 mm; Brink et al.,
2012), which again would fit a rather longer maxilla than
measured in UA 31. As appropriately noted by Brink et al. (2012),
African Middle Pleistocene molar crowns tend to show larger BL
diameters compared with their European counterparts and, with
few exceptions, almost invariably smaller MD lengths compared
with early Homo.
The fossiliferous area of Buia and the early Middle Pleistocene
site of Tighenif, Algeria, are nearly 4550 km and likely less than 300
kyr apart (Geraads et al., 1986). Recently re-attributed to
H. heidelbergensis (Mounier et al., 2009; but see; Antón, 2013) and
assessed for their inner structural morphology (Zanolli et al., 2010;
Zanolli and Mazurier, 2013), the teeth from Tighenif share a number
of features with the Eritrean specimens. With respect to the UA 369
lower I1, at the external surface these include the BL diameter and
the lack of enamel superstructures. Conversely, the isolated North
African lower I1 differs because of its relatively thicker enamel
(notably, on the lingual aspect) and radicular dentine (notably,
labially), and mostly for its spatula-shaped (versus a labiolingually
compressed outline) pulp cavity at crown level, which turns into a
regularly-shaped (versus an ovoid-shaped) cross-section along the
entire radicular portion. Compared with the lower M1s and M2s of
Tighenif, the MA 93 crown from Mulhuli-Amo mostly shares a
medium-large hypoconulid, presence of a small tuberculum intermedium (because of occlusal wear, only visible at the EDJ level on
Tighenif 2, but not present in Tighenif 1), an occlusal groove pattern
(with the lower M2 of Tighenif 2, but not with the lower M1), a
percentage of coronal volume that is dentine and pulp (Vcdp/Vc),
and similarly thickened enamel (2e3D RET values). However, the
Eritrean and Algerian molars differ in crown shape (more buccolingually expanded in Tighenif), mid-trigonid crest pattern
expressed at the EDJ (of middleemiddle type in Tighenif), and details of the EDJ conformation (rather low dentine horns in MA 93),
C. Zanolli et al. / Journal of Human Evolution 74 (2014) 96e113
with Tighenif’s lower M2s more closely approaching the modern
human condition (Zanolli and Mazurier, 2013).
As a whole, while quantitatively limited, comparative evidence
from Buia/Mulhuli-Amo and Tighenif indicates a blend of primitive
(mostly found in the earlier Danakil specimens), derived (mostly
found in the later Algerian assemblage), and unique features
pointing to a significant degree of tooth variation at a macroregional scale and to a likely nonlinear pattern of dental morphostructural evolution across the Early to Middle Pleistocene. In this
respect, while 2e3D virtual tooth imaging potentially discloses
new promising perspectives in inter-taxic comparisons (e.g., Smith
et al., 2012; Liu et al., 2013; Macchiarelli et al., 2013), we admit that
the current paucity of similar evidence from more representative
Early and Middle Pleistocene African assemblages still limits any
reliable conclusion about the variation patterns and evolutionary
trends in H. erectus/ergaster tooth endostructural morphology. This
in turn reduces the chances of providing conclusive, dentally-based
support to the suggested speciation event occurring in Africa during the early Middle Pleistocene (Rightmire, 2013). This emphasises
the importance of continually developing methods, especially
those that are non-desctructive, to extract more information out of
the existing fossil record (Wood and Leakey, 2011).
Acknowledgements
The Buia Project (Eritrean-Italian Danakil Expedition: AnthropoArchaeological and Geo-Paleontological Research Project), an
ongoing international project developed in agreement and collaboration with the Eritrean National Museum of Asmara and the Northern
Red Sea Regional Museum of Massawa, is granted by the Italian
Ministry for Education and Research (COFIN and PRIN national projects), the Italian Ministry for Foreign Affairs (DGPCC-V; grants ARC000387/2011, ARC-000504/2012, ARC-000853/2013), the University
‘La Sapienza’ of Rome (‘Grandi Scavi Archeologici’ project; grant
B88C13003900005 and B88C13000440005). During the last years,
our field work has also benefited from the support provided by the
Italian National Research Council, the University of Florence, the
Leakey Foundation, the National Geographic Society, the Spanish
Ministry of Science and Education, the National Museum of Prehistory
and Ethnography of Rome, the University of Poitiers, the French CNRS
(MNHN Paris). For scientific collaboration, we acknowledge E. Abbate
(Florence), M.G. Belcastro (Bologna), P. Bruni (Florence), G. Carnevale
(Turin), M. Delfino (Turin), M. Ghinassi (Pavia), B. Martínez-Navarro
(Tarragona), A. Mazurier (Poitiers), P. O’Higgins (York), O. Oms (Barcelona), M. Papini (Florence), M. Pavia (Turin), M. Sagri (Florence). We
are also grateful to F. Bernardini (Trieste), M. Chech (Paris), F. Genchi
(Bologna), A. Keset (Massawa), N. Kiflemariam (Massawa), F. Romagnoli (Florence), D. Tesfay (Massawa), A. Todero (Bologna), P. Ungar
(Fayetteville), V. Vannata (Rome), and A. Zerai (Asmara). Very useful
and competent comments were provided by one referee when commenting on the comparative evidence from Atapuerca. For detailed
stratigraphic information about the Mulhuli-Amo site, we especially
thank M. Ghinassi and M. Papini. The specimen MA 93 was collected in
2011 by the Saho guide Hussein Umar. Finally, we recognize that
without the generous help and warm hospitality of the people from
the Buia village, this work would simply have not been possible.
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