Behavioral inferences from the high levels of dental chipping in Homo naledi

Abstract

Objectives:
A variety of mechanical processes can result in antemortem dental chipping. In this study, chipping data in the teeth of Homo naledi are compared with those of other pertinent dental samples to give insight into their etiology.

Materials and methods:
Permanent teeth with complete crowns evidencing occlusal wear were examined macroscopically. The location, number, and severity of fractures were recorded and compared to those found in samples of two other South African fossil hominin species and in samples of nonhuman primates (n = 3) and recent humans (n = 7).

Results:
With 44% of teeth affected, H. naledi exhibits far higher rates of chipping than the other fossil hominin samples. Specifically, 50% of posterior teeth and 31% of anterior teeth display at least one chip. The maxillary teeth are more affected than the mandibular teeth (45% vs 43%, respectively), 73% of molar chipping occurs on interproximal surfaces, and right teeth are more often affected than left teeth (50% vs 38%).

Discussion:
Results indicate that the teeth of H. naledi were exposed to acute trauma on a regular basis. Because interproximal areas are more affected than buccal and posterior teeth more than anterior, it is unlikely that nonmasticatory cultural behavior was the cause. A diet containing hard and resistant food, or contaminants such as grit, is more likely. The small chip size, and steep occlusal wear and cupped dentine on some molars are supportive of the latter possibility. This pattern of chipping suggests that H. naledi differed considerably-in terms of diet, environment, and/or specialized masticatory processing-relative to other African fossil hominins.

Full text

BRIEF COMMUNICATION
Behavioral inferences from the high levels of dental chipping in
Homo naledi
Ian Towle
1
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Joel D. Irish
1,2
|
Isabelle De Groote
1
1
Research Centre in Evolutionary
Anthropology and Palaeoecology, School of
Natural Sciences and Psychology, John
Moores University, Liverpool L3 3AF, United
Kingdom
2
Evolutionary Studies Institute and Centre
for Excellence in PaleoSciences, University
of the Witwatersrand, Private Bag 3, WITS
2050, South Africa
Correspondence
Ian Towle, Room 352, James Parsons
Building, Byrom Street, Liverpool L3 3AF,
United Kingdom.
Email: I.Towle@2014.ljmu.ac.uk
Funding information
Liverpool John Moores University
Abstract
Objectives: A variety of mechanical processes can result in antemortem dental chipping. In this
study, chipping data in the teeth of Homo naledi are compared with those of other pertinent dental
samples to give insight into their etiology.
Materials and methods: Permanent teeth with complete crowns evidencing occlusal wear were
examined macroscopically. The location, number, and severity of fractures were recorded and
compared to those found in samples of two other South African fossil hominin species and in sam-
ples of nonhuman primates (n53) and recent humans (n57).
Results: With 44% of teeth affected, H. naledi exhibits far higher rates of chipping than the other
fossil hominin samples. Specifically, 50% of posterior teeth and 31% of anterior teeth display at
least one chip. The maxillary teeth are more affected than the mandibular teeth (45% vs 43%,
respectively), 73% of molar chipping occurs on interproximal surfaces, and right teeth are more
often affected than left teeth (50% vs 38%).
Discussion: Results indicate that the teeth of H. naledi were exposed to acute trauma on a regular
basis. Because interproximal areas are more affected than buccal and posterior teeth more than
anterior, it is unlikely that nonmasticatory cultural behavior was the cause. A diet containing hard
and resistant food, or contaminants such as grit, is more likely. The small chip size, and steep occlu-
sal wear and cupped dentine on some molars are supportive of the latter possibility. This pattern
of chipping suggests that H. naledi differed considerably—in terms of diet, environment, and/or
specialized masticatory processing—relative to other African fossil hominins.
KEYWORDS
dental fractures, enamel, hominin diet, South Africa
1
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INTRODUCTION
Antemortem dental chipping occurs when a tooth contacts a hard
object with enough force to fracture the enamel (Chai & Lawn, 2007;
Constantino et al., 2010), in a process akin to pressure flaking of stone
tools. Fracture can occur with minimal plastic deformation because
enamel is strong but brittle (Thomas, 2000). For example, in the human
dentition, enamel can withstand pressures >1000 N, equating to con-
tact stress of up to 2.5 GPa; however, the fracture point varies depend-
ing on the properties of both the enamel and the object making
contact with the enamel (Constantino et al., 2010; He & Swain, 2008;
Lawn, Lee, Constantino, & Lucas, 2009; Scott & Winn, 2011). Chipping
differs from other types of crown wear in that it is not a gradual pro-
cess and does not leave a smooth occlusal surface. Irregular breaks are
created on the occlusal edge of the enamel, though they may reach the
dentine in severe cases. Such data therefore can offer some insight
into the diet and behavior of past individuals and populations, espe-
cially because it often takes many years of subsequent attrition and
abrasion to erase chips (Constantino, Markham, & Lucas, 2012). Chip-
ping has been recorded in a range of different mammals, with consider-
able variation in the patterns and causes of fractures, which include
food processing, accidents, diet, environmental contaminants, and
social behavior (Constantino et al., 2012; Sauther, Sussman, & Cuozzo,
2002; Scott & Winn, 2011; Stojanowski, Johnson, Paul, & Carver,
Am J Phys Anthropol.2017;1–9. wileyonlinelibrary.com/journal/ajpa V
C2017 Wiley Periodicals, Inc.
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1
Received: 9 December 2016
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Revised: 3 May 2017
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Accepted: 4 May 2017
DOI: 10.1002/ajpa.23250

2015; Van Valkenburgh, 2009). Different dietary items cause enamel
fractures at different rates and sizes, from soft fruits that rarely cause
chipping to hard seeds and nuts that may lead to large chips. However,
the propensity of some foods for dental chipping is more difficult to
discern. Bark and low-quality terrestrial herbaceous vegetation tend to
envelop the crown surface, thereby spreading out stresses to make
chipping unlikely (Chai, Lee, Kwon, Lucas, & Lawn, 2009; Lucas,
Constantino, Wood, & Lawn, 2008). Environmental contaminants may
also be important, such as grit incorporated into the diet (Belcastro
et al., 2007; Nystrom, Phillips-Conroy, & Jolly, 2004). The size and
shape that an object must be to cause chipping are subjects of debate
(e.g., Constantino et al., 2012; Daegling et al., 2013; Lucas et al., 2008);
yet, the teeth affected, position on the tooth, and severity can all give
insight into the etiology producing such chips (Belcastro et al., 2007;
Constantino et al., 2010; Scott & Winn, 2011).
Comparatively low chipping rates are found in gorillas and chim-
panzees relative to orangutans (Constantino et al., 2012). The rate in
gorillas is a result of their infrequent ingestion of hard seeds and fruits,
while feeding predominantly on foods like low-quality herbaceous veg-
etation (Conklin-Brittain, Knott, & Wrangham, 2001; Doran et al.,
2002). Similarly, chimpanzees commonly consume soft fruits (Conklin-
Brittain et al., 2001). Orangutans, however, have far higher chipping
rates than other great apes, with Constantino et al. (2012) reporting
three to six times more chips on their posterior teeth. This high rate is
attributed to the large hard foods that make up a significant part of
their diet (Galdikas, 1982).
A variety of recent human populations have also been studied
(e.g., Belcastro et al., 2007; Bonfiglioli, Mariotti, Facchini, Belcastro, &
Condemi, 2004; Gould, 1968; Lous, 1970; Molnar et al., 1972; Scott &
Winn, 2011; Silva, Gil, Soares, & da Silva, 2016; Turner & Cadien,
1969), and the findings are useful for inferring chipping etiologies in
fossil hominins. In general, hunter-gatherers tend to have higher rates
in their posterior teeth, whereas agriculturalists have more chipping of
the anterior teeth. In addition, the former groups are most affected by
diet or environmental contaminants, while the latter are more often
affected by diet and tool use (Scott & Winn, 2011; Stojanowski et al.,
2015). Nonmasticatory behavior is usually the focus of chipping studies
in Homo sapiens, with different activities leading to a variety of patterns
(e.g., Bonfiglioli et al., 2004; Gould, 1968; Larsen, 2015; Lous, 1970;
Molnar et al., 1972).
Chipping frequencies have also been recorded in hominin fossils,
with South African specimens particularly well studied (Constantino
et al., 2010; Grine et al., 2010; Robinson, 1954; Tobias, 1967). For
example, there has been much debate in the literature concerning what
the frequencies of dental chipping in Paranthropus robustus and
Australopithecus africanus indicate in terms of diet. Alternate explana-
tions include grit introduced into the masticatory process from eating
roots (Robinson, 1954), crunching of bones (Tobias, 1967), and con-
sumption of seeds and nuts (Constantino et al., 2010). Chipping has
also been noted in the teeth of A. afarensis (Johanson & Taieb, 1976),
Australopithicus anamensis (Ward, Leakey, & Walker, 2001),
Paranthropus boisei (Tobias, 1967), and Homo neanderthalensis (Fox &
Frayer, 1997). Neanderthal teeth exhibit high rates that are likely
caused, at least in part, by nonmasticatory processes (Fiorenza &
Kullmer, 2013; Fox & Frayer, 1997).
Although dental chipping can be useful in reconstructing hominin
diets, a few issues have not yet been thoroughly addressed in the liter-
ature, including the effects that enamel microstructure, thickness, and
morphology have on susceptibility to fracture, and the time spent in
occlusion and wear of the tooth. It has been suggested that fractures
may follow lines of weakness such as lamellae and tufts, which means
cracks can form differentially or more easily at certain locations (Lucas
et al., 2008). Similarly, orientation of enamel microstructure, as well as
the dietary object is important (Xu et al., 1998). Most research on frac-
tures assumes that enamel has similar properties across the occlusal
surface, as well as between tooth types and populations. However,
more recent work suggests that enamel mechanical properties differ
across the surface of a single tooth, and between teeth (Cuy, Mann,
Livi, Teaford, & Weihs, 2002; Macho & Shimizu, 2009; Ziscovici, Lucas,
Constantino, Bromage, & Van Casteren, 2014). Enamel property differ-
ences among species could also mean that two closely related species
with nearly identical diets have markedly different patterns of chipping.
In this regard, it was proposed that thick enamel may have evolved in
certain lineages to resist tooth loss through fracture (Kay, 1981; Lucas
et al., 2008). This possibility could lead to bias in the data if these same
species evolved other adaptations to cope with consuming large
amounts of hard foods. Efforts to quantify bite forces in extinct species
may be especially influenced by such factors (Chai & Lawn, 2007; Chai,
Lee, & Lawn, 2011; Constantino et al., 2010; Constantino et al., 2012).
However, species differences are just beginning to be researched (e.g.,
Ziscovici et al., 2014). There are also issues concerning how samples
are chosen, such as the inclusion of incomplete crowns and differences
in the presentation of results that may yield substantial differences
among studies of the same species (Daegling et al., 2013).
That said, if care is taken in choosing the methods and enamel
property differences are considered, dental chipping should be able to
provide some insight into the diet and behavior of extinct species. By
recording position, severity, and frequency, a unique sample-specific
pattern may be obtained for comparison with other samples. In this
study, chipping data were recorded in the permanent teeth of Homo
naledi for comparison with other samples of South African fossil homi-
nins, as well as extant primates and recent humans. The results help to
characterize further the newly-defined species from South Africa’s Ris-
ing Star cave system, along with other publications (e.g., Feuerriegel
et al., 2016; Harcourt-Smith et al., 2015; Kivell et al, 2015; Williams,
Garcia-Martinez, Bastir, & Berger, 2017), several of which also concern
the teeth (Berger et al., 2015; Cofran, Skinner, & Walker, 2016;
Skinner, Lockey, Gunz, Hawks, & Delezene, 2016).
2
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MATERIALS AND METHODS
At the time of data collection, over 1,500 H. naledi specimens were
available for study, from which 15 individuals are represented (Berger
et al., 2015; Dirks et al., 2015). This material was subsequently dated
2
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TOWLE ET AL.

to c. 335-236 kya (Dirks et al., 2017). The dental sample itself consists
of 156 permanent teeth from the cave's Dinaledi Chamber, all of which
were observed directly by the first author. Following Daegling et al.
(2013), 6 damaged teeth and 24 others not subject to chipping, due to
noneruption or limited occlusion (based on negligible or no crown
wear), were not recorded. Thus, data in 126 teeth were employed for
comparison with the other samples (Table 1). The same criteria for
tooth exclusion were followed when recording chipping in A. africanus
(n5265 teeth) and P. robustus (n5235) from South Africa, and three
extant primate species: chimpanzees (n51,991), gorillas (n51,518),
and hamadryas and olive baboons (n5760). To assess the level of
intraobserver error, 218 baboon teeth were recorded on two separate
occasions; no significant difference was detected (v
2
50.008, 1 df,
p5.927). Analogous data in seven additional samples of recent
humans were derived from the literature (refer to list in Table 2,
below); of course, interobserver error could not be determined in these
cases.
Chipping frequencies are displayed by tooth rather than by individ-
ual. As well as presenting overall frequencies, teeth are subdivided
according to the severity of occlusal wear. Extensively worn teeth are
often excluded from study over concerns that previous chips have
worn away or the enamel has become more susceptible to chipping
(Bonfiglioli et al., 2004; Scott & Winn, 2011). However, this strategy
can omit important dietary trends, particularly when comparing species.
Occlusal wear is a normal part of the masticatory process, so eliminat-
ing from consideration data on teeth worn past a certain point may
mask dietary differences.
Wear data for molars were scored in accordance with the method
of Scott (1979), and for all other teeth the method of Smith (1984).
This approach was employed to determine whether dental attrition is
related to chipping frequencies. Scott’s (1979) method divides teeth
into quadrants, where each quadrant is given a score from 1 to 10. The
former value refers to a tooth that is unworn or has very small wear
facets, while the latter describes complete loss of the enamel. Smith’s
(1984) method is similar, but uses a scale of 1–8. In this study, molars
are separated from the other teeth based on the total of their four
quadrants into categories of high (i.e., 201), medium (13–19), and low
wear (5–12). Anterior teeth, here including premolars, are divided into
high (51), and medium-to-low wear (2–4) categories. If a tooth is listed
as grade 1 for either method, it was not included in the analysis due to
the likelihood it was not in occlusion. Statistical significance was tested
between tooth groups using a v
2
test of homogeneity, with significance
set at the 0.05 alpha level.
Teeth were observed macroscopically with a 103hand lens to
determine whether a chip occurred antemortem or postmortem. Dis-
tinguishing between postmortem and antemortem fractures was based
on criteria of Scott & Winn (2011), where only chips evidencing subse-
quent attrition were included in the latter category. The severity, posi-
tion, and number of chips were also recorded. Severity is based on the
three-point scale of Bonfiglioli et al. (2004): (1) slight crack or fracture
up to 0.5 mm in width or larger, but with only superficial enamel loss,
(2) larger irregular fracture up to 1 mm with the enamel more deeply
involved, and (3) chip larger than 1 mm involving both enamel and den-
tine. The number of chips per tooth was recorded following Belcastro
et al. (2007). Position was recorded as buccal, lingual, mesial, and distal.
If multiple chips are present, then the tooth surface with the most frac-
tures was recorded, whereas if the number is equal between two or
more sides, then the surface with the largest chip was recorded.
H. naledi individuals referred to in the original publication (Berger et al.,
2015) and those defined as likely individuals at the time of data collec-
tion were included.
3
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RESULTS
With 44.4% of permanent teeth affected (Table 1), H. naledi exhibits a
far higher chipping rate than the other South African samples (Table 2).
Specifically, 53.7% of molars, 44.4% of premolars, 25% of canines, and
33.3% of incisors have at least one chip; of these, 50% display two or
more chips (Figure 1 and Table 3). Only 13.6% of primary teeth are
affected. Most chips are small, that is, severity 1 (n551), with only six
recorded as 2 or 3. Over 73% of those on the molars are located inter-
proximally. Particularly common are several small chips above the wear
facets of posterior teeth (Figure 2).
Chipping frequencies are presented by wear score and side in
Table 1. Among other variation evident in these categories, it can be
seen that right teeth are affected slightly more often than left, with
rates of 50% and 37.7%, respectively, having at least one chip. The
average affected right molar has 2.37 chips and the left 2.06, with
medians of 2 and 1 in these non-normally distributed data (Shapiro–
Wilk, p5.000). However, differences by side are not statistically signif-
icant (X
2
51.945, 1 df, p5.16). Of the 12 individuals represented by
dental remains, nine have at least one chipped tooth; two of the
remaining three are represented by only one tooth, and the third has
minimally worn teeth (i.e., scores of <2).
TABLE 1 Chipping frequencies for different tooth types in H.
naledi
Sample
Total
teeth
With
chipping %
All teeth 126 56 44.44
Left teeth 61 23 37.70
Right teeth 66 33 50.00
Primary teeth 22 3 13.64
Molar wear stage
a
All molars 54 29 53.70
Light wear (5–12) 19 4 21.05
Medium wear (13–19) 21 12 57.14
High wear (201) 14 13 92.86
PMs, Cs, and Is wear stage
a
All anterior and premolar teeth 72 27 37.50
Light wear (2–4) 46 15 32.61
Heavy wear (51) 26 12 46.15
a
Molar wear is calculated following Scott (1979) with all other teeth
using Smith (1984).
TOWLE ET AL.
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3

The posterior teeth of H. naledi have more chips than the anterior
teeth, and the average difference in overall frequency is statistically sig-
nificant (v
2
53.938, 1 df, p5.047). Posterior teeth are also more likely
to exhibit multiple chips than anterior teeth; to test this, a chi-square
test was again used, though with Yates’continuity correction because
expected cell size for anterior teeth with multiple chips is 5. The dif-
ference is significant (v
2c
57.240, 1 df, p5.007).
Last, Tables 2 and 3 compare H. naledi with samples of other South
African hominins, extant primates, and recent humans. Overall chipping
rates, as well as ratios comparing chip frequency are provided for max-
illary vs. mandibular teeth, posterior vs. anterior teeth, and small vs.
large chips (Table 2). H. naledi has a higher rate of chipping than other
South African hominins and extant nonhuman primates (Table 3). The
rate is more comparable to several of the recent human samples. How-
ever, many of the latter differ in chipping ratios compared to H. naledi;
particularly noticeable is the preponderance of small chips versus large
(i.e., ratio of 8.33:1) and fewer affected anterior vs. posterior teeth
(0.61:1). Although the overall rate of chipping in H. naledi is more simi-
lar to these recent human groups, the nature of the chipping with
regard to size and location within the dental arcade is more like that
observed in A. africanus and in baboons.
4
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DISCUSSION
The H. naledi sample appears quite homogeneous with regard to the
location, number, and severity of chipping across individuals, not unlike
that of the species’developmental attributes, such as uniformly simple
crown morphology on relatively small, thick-enameled teeth (Berger
et al., 2015; Cofran et al., 2016; Skinner et al., 2016). The amount of
antemortem dental chipping across the sample, including multiple
instances in individuals with greater attrition, indicates that the teeth
were exposed to acute trauma on a regular basis. Interproximal surfa-
ces are more affected than buccal surfaces and posterior teeth more
than anterior teeth, which is suggestive of a dietary rather than a non-
masticatory cause (Belcastro et al., 2007). This patterning can result
from contaminants in the diet, like grit when consuming such foods as
roots and tubers (Belcastro et al., 2007; Robinson, 1963; Stojanowski
et al., 2015).
Clearly, there will be a point when an object is too small to create
a visible chip and instead results in enamel microwear. The point at
which this occurs likely varies, depending on the properties and shape
of both the enamel and the object (Daegling et al., 2013). The contami-
nants consumed by H. naledi would have had to at least occasionally
been above this size threshold. Certain environments make contami-
nants more likely to be consumed, such as dry and arid conditions or
areas affected by such phenomena as ash clouds following a volcanic
FIGURE 1 Chipping rates (%) for extant primates and fossil
hominins, divided by jaw and tooth type
FIGURE 2 Chipping examples: (a) U.W. 101–525 upper right first
molar, three chips on mesial surface; (b) U.W. 101–1401 upper
right second premolar, multiple small chips on distal surface;
(c) U.W. 101–1402 upper right first premolar, mesial chip. Scale is
in millimeters
4
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TOWLE ET AL.

eruption (Belcastro et al., 2007; Riede & Wheeler, 2009; Spradley,
Glander, & Kay, 2016). It will therefore be useful to incorporate data
about the environment in which H. naledi lived.
As mentioned in the Introduction, the effects of enamel thickness,
occlusal wear, and enamel microstructure on chipping frequencies are
not well understood at present. It has been suggested that thickness is
not important in terms of chip number (Constantino et al., 2012).
Nevertheless, thicker enamel can accommodate larger chips and hence
may skew inferences drawn from assessments of chip size. Severe
wear will have a similar effect on frequencies, with chip size being lim-
ited. These factors do not seem to be responsible for small chips in this
sample, because chip size is consistently small regardless of wear and
despite the presence of thick enamel (Skinner et al., 2016). It is also
unlikely that H. naledi has significantly different enamel microstructural
properties than other hominin species, given their presumed phyloge-
netic relationship. Additional research on masticatory and enamel prop-
erties should offer further insight into the susceptibility of these
individuals to dental fractures. Chipping rates clearly increase with
wear, due to enamel properties or, more likely, time in occlusion. How-
ever, it is clear that the high rate in this sample is not simply a conse-
quence of heavy wear, for even lightly worn teeth have far higher rates
of chipping than that observed in the other hominin samples. It seems
probable that the objects responsible for this chipping were consumed
regularly, especially given that small chips should wear away more
quickly than large chips.
Dental chipping in H. naledi differs notably from the other fossil
hominin samples examined for this study. The rate is roughly twice
that of A. africanus (44.44% vs 21.13%) and more than three times that
of P. robustus, among whom only 12.77% of teeth are affected. The
patterning of chipping also differs, particularly relative to P. robustus
(see ratios in Table 2). The low rate of chipping in P. robustus, with
comparable rates to gorillas, suggests they did not specialize in hard
object feeding. Although the chipping rate for A. africanus is substan-
tially lower than in H. naledi, it is higher than that for extant great apes
and P. robustus. Interestingly, the premolars of A. africanus are the most
affected teeth, supporting recent biomechanical analyses (Strait et al.,
2009, 2012), with this pattern not observed in the other hominins
studied.
The extant primate samples may offer more useful comparisons
for H. naledi. For example, in a microwear study by Nystrom et al.
(2004), baboons in dry environments were reported to consume large
amounts of grit. In the present, combined sample of hamadryas and
olive baboons, we found similarities to H. naledi, with frequent small
chips and a higher rate of chipping among posterior teeth relative to
anterior teeth.
Recent human samples with comparably high rates, such as the
Inuit and medieval Italian Quadrella (Table 2), have different patterns of
chipping than observed in H. naledi; either their anterior teeth are more
affected from extramasticatory activity, or all teeth evidence severe
chipping as a result of dietary and cultural behaviors (Belcastro et al.,
2007; Scott & Winn, 2011; Turner & Cadien, 1969). However, there
are some human parallels. A Late Woodland sample from Cape Cod in
the U.S.A. has a pattern like H. naledi in terms of frequency and posi-
tion (McManamon, Bradley, & Magennis, 1986). The overall frequency
is 43% and molars are reported as the tooth type most prone to chip-
ping, with interproximal surfaces most affected. Unfortunately, fre-
quencies for tooth types and positions in that study are not reported.
McManamon et al. (1986) suggest that the cause of this patterning
was the incorporation of sand, gravel, and/or shell fragment contami-
nants into the food. Another sample with somewhat similar frequencies
TABLE 2 Per-tooth chipping frequencies and ratios of dentition affected for H. naledi and comparative samples
Sample/location
Chipping
rate %
Multiple
chipped
teeth %
Small:
large
a
chip
ratio
Maxilla:
mandible
ratio
Anterior:
posterior
ratio Time period Reference
Fossil hominins
H. naledi 44.44 50.00 8.33:1
c
1.05:1 0.61:1
c
c. 335-236 kya This study
A. africanus 21.13 16.07 10.20:1
c
1.04:1 0.54:1 Plio-Pleistocene This study
P. robustus 12.77 6.67 1.73:1 0.66:1 1.25:1 Plio-Pleistocene This study
Extant primates
Baboons 25.26 18.75 5.40:1
c
0.79:1 0.93:1 19th/20th century CE This study
Gorillas 11.13 4.14 10.27:1
c
1.48:1
c
0.51:1
c
19th/20th century CE This study
Chimpanzees 4.92 2.04 2.27:1
c
1.73:1 0.95:1 19th/20th century CE This study
Recent humans
St. Lawrence Island Inuit 66.40
bb
1.04:1 0.77:1
c
2nd–17th century CE Scott and Winn (2011)
Quadrella (Italy) 48.40
b
0.70:1 1.14:1 1.50:1
c
2nd–3rd century BCE Belcastro et al. (2007)
Vicenne-Campochiaro (Italy) 38.90
b
1.12:1 1.17:1 1.68:1
c
4th–10th century CE Belcastro et al. (2007)
Taforalt (Morocco) 29.20
bbb
0.64:1
c
11,000–12,000 BP Bonfiglioli et al. (2004)
Norway 21.90
bb
1.24:1
c
3.40:1
c
11th–14th century CE Scott and Winn (2011)
Spain 5.90
bb
1.73:1 3.10:1
c
11th–18th century CE Scott and Winn (2011)
Cape Cod Woodland (USA) 43.40
bb
0.79:1
b
5th–10th century CE McManamon et al. (1986)
a
Small chips are those recorded as severity grade 1 and large as grades 2–3, according to Bonfiglioli et al. (2004).
b
Data not reported in publication.
c
Chi-square significant at 0.05 level.
TOWLE ET AL.
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5

TABLE 3 Chipping presence, absence, and severity for upper molars (UM), upper premolars (UP), upper canines (UC), upper incisors (UI),
lower molars (LM), lower premolars (LP), lower canines (LC), lower incisors (LI), and all teeth (All)
Sample UM % UP % UC % UI % LM % LP % LC % LI % All %
Chimpanzees
Total number of teeth
a
501 292 136 315 497 300 140 320 2501
Complete teeth with chip(s) 29 6 9 11 25 5 5 8 98
Complete teeth with no chips 415 248 107 261 432 279 121 278 2141
Damaged/incomplete teeth 57 38 20 43 40 16 14 34 262
Teeth with a wear score of 1 24 51 23 26 17 51 24 32 248
Small chips
b
19 66 5 83 6 67 9 82 16 64 3 60 2 40 8 100 68 69
Medium chips
b
10 34 1 17 2 22 2 18 9 36 2 40 3 60 0 0 29 30
Large chips
b
000011100000000001 1
Chipping frequency % 7 3 10 4 6 2 5 3 5
Gorillas
Total number of teeth
a
409 247 110 271 411 241 113 288 2090
Complete teeth with chip(s) 72 9 6 12 37 19 6 8 169
Complete teeth with no chips 301 201 78 200 332 200 83 217 1612
Damaged/incomplete teeth 36 37 26 59 42 22 24 63 309
Teeth with a wear score of 1 17 54 23 43 32 24 25 45 263
Small chips
b
68 94 7 78 6 100 8 67 33 89 18 95 6 100 8 100 154 91
Medium chips
b
4611100433411150000148
Large chips
b
001110000000000001 1
Chipping frequency % 20 6 10 7 11 10 9 4 11
Baboons
Total number of teeth
a
174 116 49 107 166 110 49 112 883
Complete teeth with chip(s) 38 16 1 29 62 10 3 33 192
Complete teeth with no chips 123 90 41 59 85 80 43 77 598
Damaged/incomplete teeth 13 10 7 19 19 20 3 2 93
Teeth with a wear score of 1 5 8 8 0 4 1 4 0 30
Small chips
b
31 82 13 81 1 100 27 93 49 79 9 90 3 100 29 88 162 84
Medium chips
b
71831900271321110004123016
Large chips
b
00000000000000000 0
Chipping frequency % 24 16 3 33 43 11 7 30 25
Paranthropus robustus
Total number of teeth
a
78 63 15 38 117 58 10 23 402
Complete teeth with chip(s) 2 4 2 3 12 5 1 1 30
Complete teeth with no chips 50 30 7 26 74 34 4 15 240
Damaged/incomplete teeth 26 29 6 9 31 19 5 7 132
Teeth with a wear score of 1 4 4 1 5 12 2 2 5 35
Small chips
b
2 100 1 25 0 0 1 33 10 83 4 80 0 0 1 100 19 63
Medium chips
b
0 0 3 75 1 50 2 67 2 17 1 20 1 100 0 0 10 33
Large chips
b
000015000000000001 3
Chipping frequency % 4 13 25 13 16 14 33 9 13
Australopithecus africanus
Total number of teeth
a
81 55 20 31 153 65 36 36 477
Complete teeth with chip(s) 6 11 0 4 24 9 1 1 56
Complete teeth with no chips 48 24 16 19 90 36 19 22 274
Damaged/incomplete teeth 27 20 4 8 39 20 16 13 147
Teeth with a wear score of 1 4 9 8 10 10 8 8 8 65
Small chips
b
6 100 10 91 0 0 4 100 22 92 8 89 0 0 1 100 51 91
Medium chips
b
00190000141111100004 7
Large chips
b
00000000140000001 2
Chipping frequency % 12 42 0 31 23 24 8 7 21
Homo naledi
Total number of teeth
a
31 21 13 14 28 19 11 19 156
Complete teeth with chip(s) 15 9 3 3 14 7 0 5 56
Complete teeth with no chips 16 11 9 11 14 11 10 12 94
Damaged/incomplete teeth 0 1 1 0 0 1 1 2 6
Teeth with a wear score of 1 2 2 4 3 3 0 6 4 24
Small chips
b
13 87 9 100 3 100 3 100 11 79 6 86 0 0 5 100 50 89
Medium chips
b
2130000003210000005 9
Large chips
b
000000000011400001 2
Chipping frequency % 52 50 38 27 56 39 0 38 44
a
Damaged/incomplete teeth and teeth with a wear score of 1 dropped from the total number of teeth before chipping frequency is calculated.
b
Small, medium, and large chips are scored according to Bonfiglioli et al. (2004) with three-point severity scale.
6
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TOWLE ET AL.

to H. naledi is from the site of Taforalt. Bonfiglioli et al. (2004) con-
cluded that the frequent interproximal chipping in these epipalaeolithic
Moroccans was due to chewing hard, abrasive snail shells and fruit
stones. Many seeds and nuts were also consumed (Humphrey et al.,
2014). Dietary contaminants may also have been a factor, given the
environmental conditions and presence of grindstones (Humphrey
et al., 2014). However, direct comparison is confounded, because these
peoples practiced maxillary incisor avulsion (De Groote & Humphrey,
2016). Last, the medieval Vicenne–Campochiaro sample exhibits a
chipping pattern similar to H. naledi; it has high rates of interproximal
chipping on posterior teeth, especially in females. Belcastro et al.
(2007) suggest the cause was grit incorporated into the diet.
If a specific food item is responsible for chipping in H. naledi,then
these individuals must have specialized in the consumption of a partic-
ular type of very small hard object. Additional evidence, to be detailed
in separate study, includes steeply-angled wear and slight cupped, that
is, scooped-out, wear of dentine on several posterior teeth in H. naledi
—both of which can result from consumption of grit, generally in con-
junction with softer foods (Brace, 1962; Hinton, 1981; Smith, 1984;
Figure 3). It also cannot be ruled out that these individuals were proc-
essing foods, at least to the extent seen in chimpanzees who dismantle
seeds and nuts before ingestion (Boesch & Boesch, 1982; Daegling
et al., 2013; Wrangham & Conklin-Brittain, 2003). So, potentially, only
small hard objects were masticated in the mouth, with larger hard items
processed to some extent prior to mastication. That said, other evi-
dence for this hypothesis is lacking. Moreover, although conjectural,
perhaps the higher rate of chipping in the right teeth of H. naledi
resulted from preferential placement of the food or objects (and con-
taminants) in this side of the mouth. Greater wear on right relative to
left teeth has been reported in several fossil Homo specimens and has
been attributed to right hand dominance in the manipulation of objects
during oral processing (Estalrrich & Rosas, 2013; Fiore, Bondioli,
Radovčić, & Frayer, 2015; Frayer et al., 2016). Yet, as noted, side differ-
ences in chipping in H. naledi were found to be nonsignificant; recovery
of additional specimens may provide clarification, while microwear and
macrowear analyses by side should provide interesting comparisons.
5
|
SUMMARY AND CONCLUSION
H. naledi exhibits high rates of antemortem enamel chipping, particu-
larly on the posterior teeth and interproximal areas. These chips are
predominately small and all individuals are affected. These characteris-
tics are suggestive of a dietary etiology rather than a nonmasticatory
cause. Once microwear analysis of the teeth by other researchers is
completed, further support may be provided for the possibility that grit
underlies the patterns of macroscopic chipping reported here. In addi-
tion, alternative forms of analyses of H. naledi specimens (e.g., photolith
analyses, etc.), along with chipping research on additional primates, par-
ticularly hominins, can help further elucidate whether H. naledi regularly
ate foods that contained contaminants. Environmental data will be of
interest to integrate. However, at present, results from this chipping
study highlight the fact that H. naledi differed noticeably from species
comprising the comparative samples studied here, in terms of diet,
behavior, and/or the environment in which they lived.
ACKNOWLEDGMENTS
The authors thank L. Berger and B. Zipfel for access to the collec-
tions at the University of the Witwatersrand, and J. Hawks and L.
Delezene for their help and advice during data collection. They also
thank I. Livne from the Powell-Cotton museum and S. Potze from
the Ditsong Museum of South Africa for access to their collections.
This research was supported by a studentship to the first author
from Liverpool John Moores University.
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How to cite this article: Towle I, Irish JD, De Groote I. Behav-
ioral inferences from the high levels of dental chipping in Homo
naledi.Am J Phys Anthropol. 2017;00:000–000. https://doi.org/
10.1002/ajpa.23250
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