Journal of Human Evolution 77 (2014) 155e166

Contents lists available at ScienceDirect

Journal of Human Evolution

journal homepage: www.elsevier.com/locate/jhevol

Food material properties and early hominin processing techniques

Katherine D. Zink a, *, Daniel E. Lieberman a, Peter W. Lucas b, 1
a
Department of Human Evolutionary Biology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA
b
Department of Anthropology, The George Washington University, 2110 G St NW, Washington, DC 20052, USA

a r t i c l e i n f o a b s t r a c t

Article history: Although early Homo is hypothesized to have used tools more than australopiths to process foods prior to
Received 23 August 2013 consumption, it is unknown how much the food processing techniques they used altered the material
Accepted 21 June 2014 properties of foods, and therefore the masticatory forces they generated, and how well they were able to
Available online 29 October 2014
comminute foods. This study presents experimental data on changes to food material properties caused
by mechanical tenderization (pounding with a stone tool) and cooking (dry roasting) of two foods likely
Keywords:
to have been important components of the hominin diet: meat and tubers. Mechanical tenderization
Diet
significantly decreased tuber toughness by 42%, but had no effect on meat toughness. Roasting signifi-
Food processing
Cooking
cantly decreased several material properties of tubers correlated with masticatory effort including
Tenderizing toughness (49%), fracture stress (28%) and elastic modulus (45%), but increased the toughness (77%),
Early Homo fracture stress (50%e222%), and elastic modulus of muscle fibers in meat (308%). Despite increasing
Oldowan many material properties of meat associated with higher masticatory forces, roasting also decreased
Fire measured energy loss by 28%, which likely makes it easier to chew. These results suggest that the use of
food processing techniques by early Homo probably differed for meat and tubers, but together would
have reduced masticatory effort, helping to relax selection to maintain large, robust faces and large,
thickly enameled teeth.
© 2014 Elsevier Ltd. All rights reserved.

Introduction
The evolution of the genus Homo is marked by reduction of the
size of the masticatory apparatus. Compared with gracile austral-
opiths, early Homo taxa (particularly Homo erectus) possessed less
robust and buttressed faces, and smaller postcanine teeth (Brace,
1967; Wolpoff, 1973; Chamberlain and Wood, 1985; McHenry,
1994; Lahr and Wright, 1996; Wood and Collard, 1999;
Lieberman, 2011). Additionally, Eng et al. (2013) have shown that
early Homo produced maximum masticatory muscle forces that
were on average 66% lower than in gracile australopiths. These
morphological changes are hypothesized to signal reduced masti-
catory effort within the genus, and are assumed to have been made
possible by a change in diet to softer foods and/or higher quality,
energetically dense foods that require fewer chews per calorie
consumed.
One often discussed dietary shift is the increased consumption
of meat by early Homo, which is supported by archaeological
* Corresponding author.
E-mail addresses: kzink@oeb.harvard.edu, danlieb@fas.harvard.edu (K.D. Zink),
peterwlucas@gmail.com (P.W. Lucas).
1 we fry, boil, bake and steam, and even modern day ‘raw foodists’
Present address: Department of Bioclinical Sciences, Faculty of Dentistry, PO
Box 24923, Safat 13110, Kuwait University, Kuwait.
evidence such as bone cut marks and stone tool remains (Bunn,
1981, 1994, 2007; Bunn and Kroll, 1986; Dominguez-Rodrigo
et al., 2002; Plummer, 2004; Dominguez-Rodrigo and Barba,
2006). Meat is a high quality food source that is calorically dense,
highly digestible, and an important source of protein and fat. From a
masticatory perspective, however, consumption of raw meat may
be a challenge. Muscle tissue comprises elastic contractile fibers
hierarchically bound by connective tissue. Under compressive,
limited-space environments like the area between occluding teeth,
meat fractures do not effectively propagate. The low-crested
bunodont molars of apes and hominins appear to be especially
poor at fracturing meat, and according to some accounts it takes
chimpanzees 4.0e11.5 h to chew small (~4 kg) animal carcasses
(Goodall, 1986; Wrangham and Conklin-Brittain, 2003). These ob-
servations suggest that increased raw meat consumption by hom-
inins may have required substantially more chewing effort, which
is inconsistent with the relatively smaller, less robust masticatory
apparatus of Homo species.
Another dietary shift that likely evolved in early Homo is
increased reliance on food processing techniques. All human pop-
ulations process much of their food before consumption
(Wrangham and Conklin-Brittain, 2003; Wrangham, 2007). Today
who eschew thermal heating of food (most of which has been

http://dx.doi.org/10.1016/j.jhevol.2014.06.012
0047-2484/© 2014 Elsevier Ltd. All rights reserved.
156 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
domesticated and is low in fiber and toxins), must expend much
effort dehydrating, pureeing, blending, juicing and soaking (Baird
and Rodwell, 2005). Although many food processing techniques
were developed within the last few thousand years, some of them,
such as simple mechanical processing and cooking, may have been
particularly important for early members of the genus Homo.
Tool use and very rudimentary forms of mechanical food pro-
cessing are not unique to humans. For example, some chimpanzee
populations use stones to pound open hard nuts (Goodall, 1986;
Boesch and Boesch-Achermann, 2000) and other animals, such as
sea otters, use stones to break open hard mollusk shells (Hall and
Schaller, 1964). It is therefore possible that the last common
ancestor of chimpanzees and hominins also practiced some form of
rudimentary processing. By the time early Homo evolved, however,
mechanical alteration of food likely became much more complex.
Stone tools date to approximately 2.6 mya (millions of years ago) in
the archeological record (Semaw et al., 1997), and may be even
older (McPherron et al., 2010). Analyses of early Oldowan sites
indicate that hominins used these stones extensively on meat and
plant material (Keeley and Toth, 1981; Semaw et al., 2003;
Dominguez-Rodrigo et al., 2005; Bunn, 2007; Pobiner et al.,
2008). Sharp edges on hand axes could have been used to slice meat
and tubers into smaller, more easily ingested particles, while other
Lower Paleolithic tools including spheroids, hammerstones and
handaxes could have been used to pound or grind food. These
different kinds of mechanical processing might have significantly
reduced masticatory effort by reducing ingested particle size and
tenderizing the food.
While it is clear then that early Homo had access to mechanical
food processing technology, the timing of cooking is much more
controversial. Wrangham et al. (1999) hypothesized that cooking
softens foods and increases net nutrient availability, helping to
make possible the evolution of larger brains and body mass com-
bined with smaller guts, teeth and less robust faces. Supporting this
hypothesis, recent research has demonstrated that cooking signif-
icantly reduces cost of digestion and increases net energy gain in
pythons and mice (Boback et al., 2007; Carmody et al., 2011). A
major problem with ascribing cooking to H. erectus, however, is a
lack of evidence for controlled fire, let alone cooking use, around
the time of early Homo. The oldest clear evidence of fire in the
archeological record is from Wonderwerk Cave dated to 1 mya
(Berna et al., 2012) and Gesher Bonet Ya'aqov at 790 kya (Goren-
Inbar et al., 2004), but hearths and other features indicative of
cooking do not appear until the Middle Paleolithic, leading many
researchers to believe that habitual cooking is a relatively recent
behavior (e.g., Brace, 1995; Ragir, 2000; Bunn, 2007; Ben-Dor et al.,
2011; Roebroeks and Villa, 2011).
Regardless of when cooking and food processing evolved, we do
not know if and by how much early processing techniques could
have permitted smaller postcanine dentition and other craniofacial
changes evident in the genus Homo. Therefore, the major goal of
this study is to provide experimental data on the material property
changes associated with Lower Paleolithic types of food processing.
Material properties describe how a food deforms, and when and
how it will fracture. These intrinsic properties govern the proba-
bility of food fracture in the oral cavity and the forces necessary to
create these fractures.
Although there is much research devoted to testing food ma-
terial properties, most studies examine the properties of raw foods
or highly processed foods such as biscuits and cheese, or they
measure the effects of harvest age, storage, chemical tenderizing,
freeze drying, etc. on properties that relate to the taste/attractive-
ness of commercial foods (e.g., Agrawal et al., 1997; Lillford, 2001;
Christensen et al., 2003; Beleia et al., 2004a; Goh et al., 2005; Sui
et al., 2006; Dominy et al., 2008; Vogel et al., 2008; Chang et al.,
2010; Duan et al., 2010; Dilek et al., 2011). In comparison, less
research has focused on the material property changes in naturally-
occurring foods caused by simple cooking or mechanical tenderi-
zation. Dominy et al. (2008) measured the material property
changes induced by roasting five species of tubers eaten by Hadza
hunter-gatherers, and the effects of boiling, steaming and/or mi-
crowave cooking is well documented for a limited number of fruits
and vegetables (e.g., Greve et al., 1994a,b; Ng and Waldron, 1997;
Thiel and Donald, 2000; Alvarez and Canet, 2001; Dan et al.,
2003; Lucas, 2004; Beleia et al., 2004a, b).
Because of commercial interest, there is extensive food property
literature on a diversity of meat types and processing methods,
including forms of mechanical (blade) tenderization. However,
most studies measure either Warner-Bratzler ‘shear forces’ (an
empirical test measuring maximum fracture force with a notched
blade) or perform a texture profile analysis (compressive tests that
assess ‘hardness’, ‘cohesiveness’, ‘springiness’ and ‘chewiness’) as
proxies for sensory perception of food by consumers (e.g., Loucks
et al., 1984; Mittal et al., 1992; Combes et al., 2003; King et al.,
2003; de Huidobro et al., 2005; Pietrasik and Shand, 2005; Dixon
et al., 2012). These are not true material properties (see below),
and therefore have limited utility for modeling food fracture within
the oral cavity. A few studies, however, have examined the material
properties of cooked meat. The most notable is Purslow (1985),
which characterized the fracture properties of beef cooked in a
water bath. This was followed by a series of papers that analyzed
muscle fiber and surrounding connective tissue responses to water-
bath cooking (Lewis and Purslow, 1989; Mutungi et al., 1995;
Willems and Purslow, 1997; Christensen et al., 2000, 2004). Un-
fortunately, all of these studies cooked the meat by boiling it in a
bag, which precisely controls cooking conditions, but likely causes
substantially less water loss than other more traditional cooking
methods relevant to human evolution.
This study builds on the existing food material property litera-
ture by measuring the changes in food material properties that
result from using two processing techniques available to early
hominins: simple mechanical tenderization (i.e., pounding with a
stone) and dry roasting. Pounding requires little effort, time or
manipulative ability and could be easily performed by any hominin
with a stone. Dry roasting requires no technology other than a fire.
Our experiments focus on tubers and meat because they were likely
two important components of hominin diets (e.g., Hatley and
Kappelman, 1980; Milton, 1999; Laden and Wrangham, 2005;
Ungar et al., 2006; Bunn, 2007). In addition, these are extremely
different foods from a materials standpoint. Raw vegetables such as
tubers comprise a latticework of cells under internal turgor pres-
sure and can be modeled as fluid-filled foams (Gibson and Ashby,
1997). In contrast, as noted earlier, raw meat is composed of
elastic contractile fibers hierarchically bound together with con-
nective tissue. It is therefore reasonable to expect that they will
respond differently to processing.
Food fracture
Before discussing the specific hypotheses tested, we first describe
a model of food fracture in the oral cavity and define the five pa-
rameters that are measured in this study: fracture stress, fracture
strain, stiffness, toughness, and energy loss. Fig. 1 shows a food item
modeled as a rigid beam between upper and lower teeth (Agrawal
et al., 1997). As the teeth come into occlusion, a stress (force per
area) is generated within the food, which deforms as it absorbs strain
energy. Initially, the food deforms elastically and will return to its
original dimensions if the occlusal force is removed (‘elastic’ defor-
mation). As stress increases, however, a yield point is reached and
any further deformation becomes permanent (‘plastic’
 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166 157

Fracture
Stress
*
Fraccture
Yield Point
*

(Force/Area)
Stress
Slope =
Modulus of Elassticity

S
Strain Fracture
(Displacemennt/Original Lengthh) Strain

Figure 1. Left: A model of food fracture between occluding teeth. Fractures can form as a result of indentation at the cusp tips (solid arrows) or from tension away from the cusps
(hatch-mark arrows). Right: A typical linear stressestrain curve. As the molars bite onto a food item, they create a stress (force/area) that induces the material to strain (proportional
deformation). Continuous application of force creates permanent deformation (yield point) and ultimately leads to the production of a fracture in the material. The slope of the
stressestrain curve is the food's modulus of elasticity, which is a measure of stiffness.

deformation). At some level of stress beyond the yield point, the food more efficient comminution (increased food breakdown per chew),
will fracture (fracture stress). Cracks can be initiated by indentation fewer chews and reduced total masticatory force.
at the cusp tips or by bending stresses distant from the cusps.
Typically, the slope of the elastic portion of the stress-strain
Hypotheses
curve defines the elastic modulus, with higher slopes indicating a
stiffer material. Although the elastic regions of these curves are
Tubers Mechanical tenderization by pounding with an Oldowan
generally linear, many foods have r-shaped stress-strain curves
hammerstone will fracture and damage the internal cellular
where the ‘r’ denotes a stress-strain curve that is concave down-
structure of tubers. Fractures in raw vegetables tend to burst cells,
wards. This curve shape is typical of stiff foods that require
which is facilitated by internal turgor pressure that pre-stresses the
disproportionate stress, compared with strain, at fracture. More
cell walls (Ng and Waldron, 1997; Thiel and Donald, 2000; Lillford,
pliant foods have stress-strain curves that are concave upwards,
2001). The elastic modulus of cell walls exceeds that of intact turgid
giving them a ‘J’ shape (Purslow, 1991a; Sui et al., 2006), and
vegetable tissue by a substantial margin and thus ‘tenderized’
typically require more strain to fracture. This difference is pertinent
vegetables may be stiffer, but the extensive fractures produced by a
to the study of oral food fracture because the limited space between
hammerstone will reduce overall toughness.
occluding teeth means that less stiff foods may not fracture as
In terms of cooking, at temperatures above 40
C pectin sub-
readily. Note that with foods possessing ‘J’ shaped stress-strain
stances are hydrolyzed and intercellular adhesion is reduced (Greve
curves, as the strain to failure approaches 0.5 or more, the defini-
et al., 1994a; Ng and Waldron, 1997; Lillford, 2001). Thus, cooking
tion of both stress and strain needs to change from its usual basis in
causes fluid to invade the intercellular space and separate the cells
the original dimensions of the object to those at the point of
(Greve et al., 1994b; Thiel and Donald, 2000; Lillford, 2001), which
measurement (Ashby and Jones, 1996).
will make roasted tubers more compliant and lower their elastic
A much more important property for food breakdown in the
modulus. Additionally, relaxed cellecell bonds and lower turgor
mouth (other than the characterization of fracture onset) is that of
pressure cause fractures in most cooked vegetables to run between
the resistance to fractures once they have initiated. The property
cells instead of through them, thereby reducing fracture resistance
that controls the progress of a fracture is toughness, quantified here
(Ng and Waldron, 1997; Lillford, 2001). Therefore, roasting tubers
as the amount of work necessary to grow a crack of a given area.
should reduce both toughness and fracture stress. Additionally,
Since most food objects have inherent flaws and weaknesses prior
cooking gelatinizes starch (Alvarez and Canet, 2001) and in higher
to being processed either orally or manually, toughness is actually
starch tubers this may further decrease fracture resistance if starch
the dominant measure of fracture force resistance in foods (as well
granules lie in the fracture path.
as in a wide range of engineering materials) (Ennos, 2012).
Meat Muscle tissue is approximately 75% water and 20% protein,
A final food parameter of importance is energy dissipation. Stiff
with the majority (~85%) of the protein component made up of
food objects, such as thick and turgid tubers, are likely to fracture in
contractile muscle fibers (myofibrillar and sarcoplasmic proteins).
bending away from cusps, but softer ones will deform and mold
The remaining protein constituent is connective tissue, which
themselves to the working surface of the teeth. In these cases, the
surrounds muscle fibers and hierarchically groups them into lon-
only option for fracture inside the mouth is cuspal penetration.
gitudinal bundles (Tornberg, 2005). Disruption of the perimysium
However, many softer, tougher foods dissipate energy internally
surrounding fiber bundles is probably the most important factor for
making it impossible to ‘run’ a crack ahead of a cusp. Thus, upper
oral processing (Purslow, 1991b). Pounding with a stone tool such
and lower teeth must eventually meet if there is to be a chance for
as an Oldowan hammerstone will mechanically disorganize the
food particle size reduction. The ability of foods to dissipate energy
uniform arrangement of the fiber bundles and may also break the
can be measured as the strain energy lost in viscous/plastic
fibers themselves. Tenderizing in this manner should therefore
behavior, which is the area within the hysteresis loop during
reduce both the fracture stress and toughness of meat.
loading-unloading cycles (Oyen-Tiesma and Cook, 2001). This
Heat denatures (unfolds) and degrades muscle proteins, dam-
measurement is particularly important for evaluating animal soft
ages cell membranes and shrinks (dehydrates) the muscle fibers
tissues such as meat, and may help to predict the probability of
(Lewis and Purslow, 1989; Tornberg, 2005). Tensile strength of meat
fracture in the oral cavity, as less energy dissipation should result in
heated in a water bath increases in two stages, from ~40 to 50
C
158 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
due to collagen denaturation, and then again from 60 to 90
C as
muscle fibers denature and shrinkage and water loss occurs, which
increases protein concentration (Lewis and Purslow, 1989;
Christensen et al., 2000; Tornberg, 2005). The morphological and
chemical changes from heating also increase muscle stiffness
(Lewis and Purslow, 1989; Tornberg, 2005) and fracture strain
(Willems and Purslow, 1997). Taken together, these effects in boiled
meat lead to the prediction that dry roasting will increase meat
toughness, fracture stress and strain, and stiffness. Increased
evaporation from open air cooking may further promote heat-
related water loss and shrinkage, leading to an even stiffer and
more fracture resistant material. As meat becomes stiffer, elastic
energy loss is reduced and toughness of the food might decrease as
less external work is required for fracture.
Mechanical processing This study also tests the general hy-
pothesis that mechanical processing of foods provides sufficient
reduction of masticatory effort to explain the smaller postcanines
of H. erectus compared with H. habilis and gracile australopiths.
Although tooth crown size varies within hominin species, post-
canine crown area was on average 21e25% smaller in H. erectus
than in H. habilis and gracile australopiths, respectively, and Homo
sapiens molars and premolars were a further 15% smaller (Brace,
1967; Wolpoff, 1973; McHenry, 1994; McHenry and Coffing,
2000). Lucas (2004) modeled postcanine occlusal area reductions
in terms of a predicted decrease in food toughness based on frac-
ture scaling. If the fracture of a food is prominently elastic, as food
affected by tenderizing or cooking probably becomes, then Lucas
(2004) predicted that dental crown size should scale with the
square root of typical food toughness. Therefore, as processing re-
duces the toughness of typical foods in the diet, a concomitant
decrease in dental occlusal area is predicted to follow, i.e., (tough-
nessprocessed food/toughnessraw food)0.5 ¼ (dental sizelater hominin/dental
sizeearlier hominin). This equation leads to the expectation that me-
chanical tenderization caused by pounding will reduce the average
toughness of foods 38e44%, allowing for the roughly 21e25%
reduction in postcanine occlusal area of H. erectus relative to
H. habilis and gracile Australopithecus species. A further reduction in
toughness on top of this (~27%) caused by cooking allowed for the
approximately 15% smaller teeth of H. sapiens. If food toughness
decreases with cooking, but not mechanical tenderization, the
argument for early adoption of cooking by H. erectus is supported.
Methods
Food samples
Organic tubers, red beets (Beta vulgaris), carrots (Daucus carota)
and jewel yams (Ipomoea batatas), were purchased from a local
store and stored at 4
C for no more than four days prior to pro-
cessing and material property testing. For the meat portion of the
experiment, an adult goat (Capra aegagrus) was purchased from a
local farm and slaughterhouse (Blood Farms, Groton, MA) and the
fresh carcass transported on ice to the Skeletal Biology Lab, Harvard
University. Muscle groups were removed using aseptic procedures,
sealed in vacuum bags and stored at 20
C. Meat was defrosted
completely at 4
C for approximately 12e24 h prior to data
collection.
Processing procedure
To limit material property variation caused by factors other than
processing, each tuber was divided into two portions (one was kept
raw, and the other was roasted or tenderized) and the same muscle
regions were used for each meat experiment (neck muscle for
toughness tests and knee flexors for the tensile tests).
Mechanical processing (tenderization) A replica of an Oldowan
hammerstone (a 560.9 g, hand-sized oval rock with smooth edges)
was used to mechanically tenderize the food. The medulla of each
tuber was sliced into 13 mm cubes, then each cube hit six times
with the hammerstone. Goat was cut into a 50 g steak and hit 20
times. This type of simple tenderization affected tubers and meat
differently. The tubers fractured into numerous, relatively large
pieces, while the meat remained intact, but was significantly
‘mashed’ and the muscle fibers disorganized where struck by the
hammerstone.
Roasting Samples were roasted on a warmed-up, tabletop pro-
pane grill (Perfect Flame™) with the lid open and the gas flow valve
set to ‘high’. Although hominins would not have used grills,
roasting in this manner is similar to an open fire (the flames are
immediately below the grill surface) and allowed cooking of mul-
tiple samples at a consistent temperature. Internal temperatures
were measured on selected samples immediately post-cooking
(tubers) or during cooking (meat) with a needle probe and digital
thermocouple (Thermoworks™, accuracy ± 0.1
C). Pre- and post-
roasted weights were recorded (digital scale, accuracy ± 0.1 g).
Before being roasted, each tuber was cut into 17 mm-thick
transverse slices. The slices were then roasted for 15.0 min, 7.5 min
on each side, with each slice rotated to a different spot on the grill
every 2.5 min during the cooking process to ensure even heating
despite grill surface temperature variations. This protocol heated
beets to 78.6 ± 2.2
C, carrots to 78.5 ± 1.1
C, and yams to
89.0 ± 2.7
C, and produced a 22 ± 3%, 27 ± 3% and 17 ± 2%
reduction in slice weight (i.e., water loss), respectively.
Two pieces of meat, one from the neck muscles (A) and the other
from the knee flexors (B), were roasted on the center of the grill.
They were periodically turned over and were cooked until ‘well-
done’ and only slightly pink internally (internal temperature,
A ¼ 72.2
C, B ¼ 76.0
C). The two steaks differed greatly in size
(Raw weight: A ¼ 67.7 g, B ¼ 331.7 g) and the larger took almost
twice as long to reach ‘well-done’ (A ¼ 24 min, B ¼ 46 min). Water
loss was similar for both steaks (A ¼ 35%, B ¼ 40%).
Material property testing
A Darvell™ HKU portable mechanical property tester (Darvell
et al., 1996) and an Instron™ 5564 were used to measure the ma-
terial properties of the food samples. Details of the particular tester
attachments that were used for each material property test can be
found within the subsections below. Tester attachments were
cleaned with alcohol between each trial. Unless noted, ten samples
of each raw, mechanically processed and roasted food type were
tested. Toughness was the only property measured for tenderized
tubers and meat because the processing procedure produced highly
fragmented pieces that precluded additional testing. Each sample
was measured with digital or dial (meat tensile tests only) calipers
(accuracy, ±0.01 and ±0.02 mm, respectively). Raw and roasted
meat samples were tested both parallel and perpendicular to fiber
direction. Because tuber material properties can change drastically
depending on the region of the food sampled, testing was only
performed on the inner region (medulla). Samples were wrapped
in damp paper towels to minimize water loss and stored in plastic
bags at 4
C until immediately before testing.
Toughness (tubers) Two experiments were performed, one
testing the effect of roasting and the other testing the effect of
mechanical tenderization. Toughness was measured using a 15

included angle wedge fitted onto the Darvell tester (100N load cell).
The wedge allows for controlled crack growth in semi-brittle foods,
such as tubers (Vincent et al., 1991).
Experiment #1. Raw and roasted tuber samples were cut into
rectangular blocks approximately 12e14 mm wide. A wedge was
 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
lowered into each sample and stopped when it just pierced the
material. At this point, the wedge was continuously lowered at a
rate of ~30 mm/min, while recording the force (F) and resulting
displacement (u) every 0.001 mm, for a final slice depth of
5.000 mm. The wedge was removed from the sample and rein-
serted into the previously formed crack to measure the work not
used in crack formation (i.e., work due to friction and elastic
bending of material against the crack faces). This work was sub-
tracted from the original work value. After testing, the length of the
crack in the horizontal plane (i.e., crack width (w)) was measured,
and toughness for each sample was calculated from when the
wedge was 2 mm into the sample to when it had progressed to a
depth of 4 mm (i.e., crack depth, m ¼ 2 mm)
(Toughness ¼ (Workinitial pass  Worksecond pass)/wu).
Experiment #2. Experimental set-up and toughness calculations
were the same as in experiment #1. The only differences were that
the samples were not a uniform size and data collection began after
the entire width of the sample was in contact with the wedge
(samples were the larger of the pieces resulting from the tenderi-
zation process and the tops were irregular). Additionally, because
they were smaller than the raw samples, maximum wedge depth
was 1.5 mm and the toughness for each tenderized piece was
calculated between a depth of 0.3 and 1.3 mm (i.e., crack depth,
u ¼ 1 mm).
Toughness (meat) Meat toughness was measured using Swis-
sors™ (Wenger, Switzerland), a pair of precision-manufactured
tailoring scissors, fitted onto the Darvell tester (100 N load cell).
Cutting tests enable measurements of controlled crack growth in
floppy (high elastic) materials such as meat (Atkins and Mai, 1979;
Lucas et al., 2001).
Using a bacon slicer, strips of raw and roasted meat of an even
2e4 mm thickness, and 12e16 mm in width, were cut. Tenderized
samples were trimmed using a razor blade and gently formed into
similar sized strips. Each sample was placed between the scissor
blades, and the handle depressed at a displacement rate of ~30 mm/
min, while recording the force (F) and resulting displacement (u)
every 0.001 mm until the sample was completely cut. The thickness
(t) and length (l) of each cut was measured and the work required
to make the cut was calculated. Work due to friction was calculated
by closing the scissors with no sample between the blades. This
work was then subtracted from the original work value to calculate
toughness (Toughness ¼ (Workinitial pass  Worksecond pass)/tl).
Compression tests (tubers) A cork borer was used to cut uniform
cylinders (radius ~3 mm, height ~8 mm) from the center of each
tuber, parallel to the long axis of the root. The radius (r) and length
(lo) of each sample was recorded. The fracture stress and strain were
then recorded by continuously compressing each sample between
two plates (displacement rate ~32 mm/min) on the Darvell tester
(1000 N load cell), recording the force (F) e displacement (u)
relationship every 0.001 mm. The data were then converted into
true stress and strain by assuming conservation of volume (i.e., a
Poisson's ratio of 0.5, a common and convenient assumption in food
analysis and supported by measurements such as those by Finney
and Hall (1967) on potato). ‘True’ stress and strain were necessary
because as failure strain approaches 0.5 or more, the definition of
both stress and strain needs to change from its usual basis in the
original dimensions of the object to those at the point of mea-
surement (Ashby and Jones, 1996). Strain was then converted to
absolute measures; a negative value obtained in the calculation
(below) signifies a compressive state. Peak stress (fracture stress)
and the corresponding strain were recorded, and the elastic
modulus (slope of the line) was calculated at 20%, 40%, 60% and 80%
fracture stress. Multiple measures are needed because a linear
stressestrain relationship is not anticipated for all foods
(Stress ¼ F(lou)/pr2lo) (Strain ¼ ln((lou)/lo)).
159
Tensile tests (meat) A bacon slicer was used to cut uniform
samples of raw and roasted meat. The thickness (t) and width (w) of
each strip (approximately 2 mm and 11 mm, respectively) were
recorded. Samples were then placed into an Instron tester (50 N
load cell) using two pneumatic grips 30 mm apart (lo) and
increasingly loaded in tension (displacement rate 90 mm/min).
Two sets of experiments were performed, a fracture test and a
cycling test. Force (F) and displacement (u) were recorded every
0.050 s for the fracture test and 0.034 s for cycling trials.
Experiment #1. Each sample was loaded until the meat had
completely fractured into two pieces. As for tubers, the force-
displacement data were converted into true stress and strain by
assuming the incompressibility of muscle in its passive state
(Van Loocke et al., 2006). Fracture stress, fracture strain and the
elastic modulus at 20%, 40%, 60% and 80% fracture stress were
recorded. One sample (raw meat, force parallel to fiber direction)
did not completely fracture and was omitted from analyses
(Stress ¼ F(lo þ u)/twlo) (Strain ¼ ln((lo þ u)/lo)).
Experiment #2. Each sample was cycled to a peak strain of 4%, 8%,
12% and 16%, and unloaded back to the initial position between
each successively large strain loop. Fractures did not initiate during
these trials. The percent work lost on unloading for each loop was
calculated. Five samples of each food type (raw and roasted, parallel
and perpendicular to muscle fiber direction) were tested.
Analyses
All calculations were performed in Excel (Microsoft 2007),
StatView statistical package (SAS Institute, version 5.0.1), and
custom written programs in LabView 8.1. In order to avoid as-
sumptions of normal distributions in the data, ManneWhitney U
tests were used to compare the raw and processed food values.
Significance was set at p  0.05.
Results
Toughness (Table 1)
Roasting reduced the toughness of tubers by 49%, from an
average of 1034 ± 345 J/m2 (raw) to 526 ± 120 J/m2 (roasted)
(p < 0.0001). Mechanically tenderizing the tubers produced a
similar result; toughness decreased 42% from 1080 ± 167 J/m2 (raw)
to 622 ± 297 J/m2 (tenderized) (p < 0.0001). Tenderization reduced
beet toughness more than roasting (tenderization ¼ 65%;
roasting ¼ 56%), while the converse was true for yams
(roasting ¼ 48%; tenderization ¼ 28%). The percent decrease in
carrot toughness was the same regardless of whether it was roasted
(39%) or tenderized (38%).
In contrast to the results for tubers, roasting increased the
toughness of meat by an average of 77% (raw average ¼ 216 ± 78 J/
m2; roasted average ¼ 381 ± 180 J/m2; p < 0.01). Toughness varied
greatly depending on whether it was measured parallel or
perpendicular to fiber direction. The former primarily measures the
toughness of the weaker connective tissues sheaths surrounding
the fibers, while the latter is a measure of the tougher muscle fibers
themselves, and although roasting increased both of these values
(raw parallel ¼ 154 ± 47 J/m2; roasted parallel ¼ 218 ± 49 J/m2;
p ¼ 0.01) (raw perpendicular ¼ 277 ± 46 J/m2; roasted
perpendicular ¼ 545 ± 84 J/m2; p < 0.001), its effect was greatest
perpendicular to fiber direction (perpendicular ¼ 97% increase;
parallel ¼ 41% increase).
Unlike with tubers, tenderizing did not affect meat toughness.
Although tenderized meat (163 ± 68 J/m2) was less tough than raw
meat measured across the muscle fibers (p < 0.01), it did not differ
significantly from the toughness of raw meat measured parallel to
160 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166

Table 1 greatest for yams (69%), followed by carrots (20%), and beets (11%).
Average toughness (J/m2) of raw, roasted and tenderized tubers and goat meat. Conversely, the average compressive strain required for fracture
Treatment Toughness (J/m2)a increased by 58%, going from 0.33 ± 0.09 in raw tubers to
Tubers, Experiment #1
0.52 ± 0.19 with roasting (p < 0.0001). As with fracture stress, the
Raw beet (n ¼ 10) 1424.9 (208.8) greatest effect was for yams (74%), although beets followed closely
Roasted beet (n ¼ 10) 622.6 (120.0) (70%). Carrot fracture strain, in comparison, increased a modest 34%
Raw carrot (n ¼ 10) 903.8 (256.0) with roasting.
Roasted carrot (n ¼ 10) 553.0 (48.1)
Inspection of the stress-strain curves for raw and roasted tubers
Raw yam (n ¼ 10) 774.6 (101.3)
Roasted yam (n ¼ 10) 403.0 (39.4) showed that the curves changed in shape from linear/slightly r-
All tubers, raw (n ¼ 30) 1034.4 (344.7) shaped (raw) to J- or even slightly s-shaped (roasted) (Fig. 2).
All tubers, roasted (n ¼ 30) 526.2 (119.8) Comparing modulus values, roasting decreased the stiffness of all
Tubers, Experiment #2
tubers (45% reduction, tuber and modulus average; p < 0.0001),
Raw beet (n ¼ 10) 922.7 (103.5)
Tenderized beet (n ¼ 10) 322.2 (90.5)
with the exception of carrots measured at 40% fracture stress (no
Raw carrot (n ¼ 10) 1239.7 (134.0) significant difference). Average raw tuber modulus started off high
Tenderized carrot (n ¼ 10) 769.1 (317.1) at 6026 ± 2087 kPa (measured at 20% fracture stress) and declined
Raw yam (n ¼ 10) 1078.5 (71.3) steadily to 4627 ± 1095 kPa (measured at 80% fracture stress). In
Tenderized yam (n ¼ 10) 773.6 (162.3)
contrast, roasted tubers followed a different pattern, starting off at a
All tubers, raw (n ¼ 30) 1080.3 (166.8)
All tubers, tenderized (n ¼ 30) 621.6 (297.1) low of 2449 ± 1332 kPa and then increasing to 3174 ± 1582 kPa,
Meatb before decreasing to 3024 ± 1535 kPa and 2629 ± 1491 kPa
Raw, parallel (n ¼ 10) 154.3 (46.5) (measured at 20%, 40%, 60% and 80% fracture stress, respectively).
Roasted, parallel (n ¼ 10) 218.2 (48.7) Yams had the greatest reduction in overall stiffness with roasting
Raw, perpendicular (n ¼ 10) 277.1 (46.3)
Roasted, perpendicular (n ¼ 10) 544.6 (84.2)
(76%), followed by carrots (31%) and beets (30%).
Tenderized (n ¼ 10)c 163.3 (68.0)
a
Toughness of tubers and meat was measured using wedge and cutting tests,
respectively. One standard deviation is in parentheses. Underlined and bolded Meat tensile tests (Table 2)
values indicate a significant difference between processed foods and their raw
counterparts (p  0.05, ManneWhitney U test). See text for food processing details. Unlike tubers, roasting increased the fracture stress of meat,
b
Meat was measured both parallel and perpendicular to muscle fiber direction. with the greatest change occurring parallel to fiber direction.
c
Toughness of tenderized meat differed significantly from raw meat measured
perpendicular, but not parallel to muscle fiber direction.
Maximum stress at fracture went from 20 ± 10 kPa (raw) to
31 ± 9 kPa (roasted), when meat was pulled perpendicular to the
direction of the fibers, primarily breaking the weaker connective
fiber direction or average raw meat toughness (average raw meat tissue rather than the fibers themselves (p ¼ 0.03). When meat was
toughness parallel and perpendicular to fiber direction, 216 ± 78 J/m2). tensed parallel to fiber direction, fracture stress rose from
96 ± 32 kPa (raw) to 309 ± 117 kPa (roasted), a 222% increase
(p < 0.001). The maximum amount of tensile deformation required
Tuber compression tests (Table 2) to fracture the meat into two separate pieces did not significantly
change with roasting (raw parallel ¼ 0.65 ± 0.16; roasted
With one exception (noted below), roasting significantly parallel ¼ 0.48 ± 0.20) (raw perpendicular ¼ 0.54 ± 0.11; roasted
affected the fracture stress, fracture strain and stiffness of tubers. In perpendicular ¼ 0.49 ± 0.12).
all cases, roasting altered yams more than carrots and beets. Roasting changed the shape of the stress-strain curve from
The stress required to fracture tubers was greatly lowered with linear or slightly J-shaped to r-shaped, but only when pulling par-
roasting, decreasing 28% from a raw average of 1349 ± 349 kPa to a allel to fiber direction (Fig. 3). Curve shape remained the same (J-
roasted average of 974 ± 555 kPa (p < 0.01). This reduction was shaped) when meat was pulled perpendicular to fiber direction,

Table 2
Average fracture stress (kPa) and strain, and modulus of elasticity (kPa) of raw and roasted tubers and goat meat.a

Treatment Fracture stress (kPa) Fracture strain Modulus at 20% Modulus at 40% Modulus at 60% Modulus at 80%
fracture stress (kPa)b fracture stress (kPa)b fracture stress (kPa)b fracture stress (kPa)b

Tubers
Raw beet (n ¼ 10) 1610.1 (130.8) 0.43 (0.05) 4579.0 (1076.3) 4090.3 (439.2) 4159.6 (431.3) 4661.9 (692.0)
Roasted beet (n ¼ 10) 1427.7 (201.0) 0.73 (0.06) 2737.8 (461.3) 3385.3 (646.0) 3311.6 (690.0) 2843.2 (1028.1)
Raw carrot (n ¼ 10) 1531.1 (199.7) 0.32 (0.03) 6816.4 (2520.0) 5982.8 (1328.4) 5659.7 (907.3) 5570.5 (866.2)
Roasted carrot (n ¼ 10) 1217.8 (299.1) 0.43 (0.07) 3527.7 (1326.8) 4674.0 (1316.7) 4498.5 (976.7) 3943.0 (1019.1)
Raw yam (n ¼ 10) 905.8 (59.0) 0.23 (0.04) 6682.3 (1740.2) 5583.7 (1237.2) 4411.7 (785.0) 3649.8 (764.9)
Roasted yam (n ¼ 10) 277.1 (166.2) 0.40 (0.18) 1081.2 (525.6) 1463.9 (337.4) 1262.9 (455.9) 1102.0 (713.6)
All tubers, raw (n ¼ 30) 1349.0 (348.5) 0.33 (0.09) 6025.9 (2087.1) 5218.9 (1330.0) 4743.7 (974.4) 4627.4 (1095.3)
All tubers, roasted (n ¼ 30) 974.2 (554.8) 0.52 (0.19) 2448.9 (1331.6) 3174.4 (1581.9) 3024.4 (1534.9) 2629.4 (1491.2)
Meatc
Raw, parallel (n ¼ 9)d 96.0 (32.4) 0.65 (0.16) 148.6 (65.4) 148.3 (47.4) 246.5 (59.7) 328.8 (106.7)
Roasted, parallel (n ¼ 10) 309.2 (116.6) 0.48 (0.20) 1066.7 (580.1) 935.7 (556.2) 822.4 (369.6) 733.6 (166.9)
Raw, perpendicular (n ¼ 10) 20.3 (9.8) 0.54 (0.11) 53.1 (41.3) 66.1 (50.0) 65.7 (52.7) 78.6 (45.6)
Roasted, perpendicular (n ¼ 10) 30.7 (8.9) 0.49 (0.12) 55.8 (20.6) 90.6 (25.3) 84.6 (40.5) 111.8 (39.4)
a
Properties of tubers and meat were measured using compression and tensile tests, respectively. One standard deviation is in parentheses. Underlined and bolded values
indicate a significant difference between raw and roasted foods (p  0.05, ManneWhitney U test). See text for food processing details.
b
Elastic modulus was measured at 20%, 40%, 60% and 80% fracture stress.
c
Meat was measured both parallel and perpendicular to muscle fiber direction.
d
One raw meat sample (measured parallel to fiber direction) did not completely fracture and was omitted from the analyses, reducing sample size to nine.
 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166 161

A A
2000 250
Beet Parallel
Parallel
1600 200
Stress (kPa)

1200

Stress (kPa)
150
800
100
400
50
0
0 0.2 0.4 0.6 0.8 1
0
Strain
0 0.1 0.2 0.3 0.4 0.5 0.6
B
2000 Strain
Carrot
1600 B
25
Stress (kPa)

Perpendicular
1200
20
800

Stress (kPa)
15
400
10
0
0 0.2 0.4 0.6 0.8 1 5
Strain
C 0
2000
Yam 0 0.1 0.2 0.3 0.4 0.5 0.6
1600 Strain
Stress (kPa)

1200 Figure 3. Average stress-strain curves of raw (light) and roasted (dark) meat. Meat was
loaded in tension both parallel (A) and perpendicular (B) to muscle fiber direction.
800

400
samples tensed to 4%, 8%, 12% and 16% strain, respectively). There
0 was no significant difference in energy loss between raw and
0 0.2 0.4 0.6 0.8 1 roasted samples pulled perpendicular to fiber direction. Although
Strain roasting had no effect, average energy loss measured in this di-
rection was relatively low and comparable to that of roasted meat
Figure 2. Representative stressestrain curves of raw (light) and roasted (dark) beets
measured parallel to fiber direction (45 ± 7% versus 45 ± 6%,
(A), carrots (B) and yams (C). Fracture occurred at the last point displayed.
respectively).

regardless of whether it was raw or roasted. A similar pattern Discussion

emerges for comparisons of stiffness. The average modulus of
roasted meat parallel to fiber direction was 308% higher than raw
meat (p < 0.001), while the modulus measured perpendicular to
fiber direction did not significantly change. Parallel to fiber direc-
tion, the raw meat modulus was unchanged at 20% and 40% fracture
stress (149 ± 65 kPa and 148 ± 47 kPa, respectively), and then
increased to 247 ± 60 kPa and 329 ± 107 kPa (measured at 60% and
80% fracture stress, respectively). The comparable roasted meat
modulus, however, steadily decreased with increasing fracture
stress, going from a high of 1067 ± 580 kPa to 936 ± 556 kPa,
822 ± 370 kPa and 734 ± 167 kPa (measured at 20%, 40%, 60% and
80% fracture stress, respectively). Regardless of whether the meat
was raw or roasted, stiffness perpendicular to the direction of the
fibers was much lower than when measured parallel to fiber di-
rection (Raw ¼ perpendicular 70% lower than parallel;
Roasted ¼ perpendicular 90% lower than parallel; p < 0.001).
Meat cycling (Table 3)
Roasting significantly decreased work loss (energy dissipation),
but only when measured parallel to fiber direction (p < 0.01)
(Fig. 4). On average, roasted samples lost 28% less energy than raw
samples (66 ± 11% versus 38 ± 3%, 74 ± 11% versus 44 ± 4%, 77 ± 10%
versus 49 ± 3%, 78 ± 9% versus 51 ± 3% for raw versus roasted
As predicted, tuber material properties responded to both me-
chanical tenderization and roasting. Tenderizing reduced tuber
toughness by 42%, and roasting reduced toughness slightly more,
49% on average. Roasting the tubers also decreased fracture stress,
made them more compliant, and increased fracture strain. In
contrast, meat did not respond as predicted for all material prop-
erty measures. Tenderizing the meat by pounding with a ham-
merstone did not change toughness, suggesting that this form of
processing simply disorganized the muscle fibers and connective
tissue without altering their intrinsic properties. Additionally,
although roasting significantly increased meat toughness, fracture
stress and stiffness, and reduced elastic energy loss, the latter two
properties responded only when measured parallel to fiber direc-
tion. Finally, contrary to predictions, roasting meat did not signifi-
cantly affect the amount of strain necessary for fracture.
What are the implications of these material property data for
the evolution of hominin mastication? The tuber results support
the hypothesis that mechanical processing could have played a role
in favoring the smaller postcanine crowns of H. erectus compared
with H. habilis and gracile australopiths. Based on fracture scaling,
which predicts that dental size is proportional to the square root of
typical food toughness (Lucas, 2004), the 42% average toughness
decrease measured in tubers pounded with a hammerstone should
162 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166

Table 3
Average percent work lost (energy dissipation) during loading-unloading cycles of raw and roasted meat.a

Parallel (n ¼ 5) Perpendicular (n ¼ 5)

Raw Roasted Raw Roasted

5 5 4 4 5 6
4% Strain Work (J), loaded 7.03  10 (2.23  10 ) 2.34  10 (1.21  10 ) 1.50  10 (9.99  10 ) 3.27  105 (1.26  105)
Work lost (J), unloaded 4.62  105 (1.77  105) 8.87  105 (4.64  105) 6.21  106 (3.49  106) 1.44  105 (6.68  106)
% Work Lostb 65.6% (11.3%) 37.9% (2.5%) 43.6% (6.8%) 43.4% (7.6%)
8% Strain Work (J), loaded 2.46  104 (6.59  105) 1.02  103 (4.93  104) 6.42  105 (4.73  105) 1.11  104 (3.76  105)
Work lost (J), unloaded 1.79  104 (4.73  105) 4.57  104 (2.26  104) 2.60  105 (2.41  105) 5.00  105 (2.35  105)
% Work lostb 73.6% (11.0%) 44.3% (4.4%) 37.9% (7.4%) 43.8% (6.8%)
12% Strain Work (J), loaded 4.64  104 (1.34  104) 2.33  103 (1.06  103) 1.53  104 (1.05  104) 2.23  104 (6.17  105)
Work lost (J), unloaded 3.48  104 (7.41  105) 1.14  103 (5.25  104) 6.37  105 (5.97  105) 1.05  104 (4.65  105)
% Work Lostb 76.9% (9.9%) 48.8% (3.4%) 37.7% (10.8%) 45.9% (8.2%)
16% Strain Work (J), loaded 6.62  104 (2.18  104) 3.90  103 (1.69  103) 2.87  104 (1.78  104) 3.55  104 (6.99  105)
Work lost (J), unloaded 5.01  104 (1.14  104) 1.99  103 (8.52  104) 1.12  104 (8.36  105) 1.73  104 (6.17  105)
% Work lostb 77.8% (8.9%) 50.9% (3.0%) 36.8% (8.6%) 47.8% (8.0%)
a
Meat was measured both parallel and perpendicular to muscle fiber direction. Each sample was successively loaded-unloaded to 4%, 8%, 12% and 16% strain. One standard
deviation in parentheses. See text for food processing details.
b
Percent work loss was calculated as the difference between the work performed during loading and unloading of the sample (i.e., work lost) divided by the work per-
formed during loading. Underlined and bolded values indicated a significant difference in percent work lost between raw and roasted meat (p  0.05, ManneWhitney U test).

result in a 24% decrease in postcanine occlusal area, a reduction that
corresponds remarkably closely with observations from the fossil
record (e.g., Brace, 1967; Wolpoff, 1973; McHenry, 1994; McHenry
and Coffing, 2000). Because pounding breaks tubers into smaller
pieces, it also reduces ingested particle size, which may have
further decreased required masticatory force.
Roasting tubers decreased toughness 17% more than tenderi-
zation. Although the average toughness difference caused by the
two processing methods was not as large as predicted from fracture
scaling (27%), the larger effect of roasting compared with tenderi-
zation suggests that habitual cooking may have contributed to the
dental size reductions and facial gracility of later Homo. It is
important to note, however, that while roasting generally reduced
the toughness of tubers more than tenderization, this result was
driven largely by the yam data; the effects of roasting on tuber
material properties were largest for yams, possibly due to a higher
internal temperature reached during cooking, and also from their
higher starch content and the presence of a unique heat-activated
beamylase that further aids starch gelatinization (Binner et al.,
2000). In contrast to yams, beet toughness was more affected by
tenderization than roasting (65% and 56% decrease, respectively),
and carrot toughness was equally affected by the two processing
methods (38% and 39% decrease, respectively). Data on additional
foods are needed before we can conclude with confidence that the
effects of cooking on tuber toughness (and masticatory force) are
superior to that of tenderization.
Agrawal et al. (1998) demonstrated a negative correlation be-
tween chewing muscle recruitment and a food's (toughness/stiff-
ness)0.5. Thus, across a wide-range of food types, foods with lower
stiffness relative to toughness are chewed with less muscular effort.
To further explore the differential effects of cooking, Table 4 presents
calculations of this index for the three tubers (N.B. this index could
not be calculated for tenderized tubers because we did not measure
the stiffness of these foods.). While (toughness/stiffness)0.5

Figure 4. Left: Average force-displacement curves for raw (light) and roasted (dark) meat. Each sample was successively loaded-unloaded to 4%, 8%, 12% and 16% strain. Right:
Percent work lost (energy dissipation) during the unloading phase of each work cycle. Meat was loaded in tension both parallel (A) and perpendicular (B) to muscle fiber direction.
Box plot whiskers extend to the 10th and 90th percentiles. *p  0.05, ManneWhitney U Test.
 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
Table 4
Ratio of the toughness and stiffness (elastic modulus) of raw and roasted tubers and
meat.a
Treatment (Toughness/Stiffness)0.5
Tubers
Raw beet (n ¼ 10) 0.57
Roasted beet (n ¼ 10) 0.45
Raw carrot (n ¼ 10) 0.39
Roasted carrot 0.36
Raw yam (n ¼ 10) 0.39
Roasted yam (n ¼ 10) 0.57
Meatb
Raw, connective tissue (n ¼ 10) 1.53
Roasted, connective tissue (n ¼ 10) 1.60
Raw, muscle fiber (n ¼ 9)c 1.13
Roasted, muscle fiber (n ¼ 10) 0.78
a 1998). Improved comminution is likely to lead to a significant
See text for experimental details. Stiffness (elastic modulus) at 20%, 40%, 60%
and 80% fracture stress was averaged.
b
Material properties of meat were measured both parallel and perpendicular to
muscle fiber direction. (Toughness/Stiffness)0.5was calculated for the properties that
primarily describe 1) the connective tissue of the meat (i.e., toughness measured
parallel to muscle fiber direction, and average stiffness measured perpendicular to
muscle fiber direction), and 2) the muscle fibers of the meat (i.e., toughness
measured perpendicular to muscle fiber direction, and average stiffness measured
parallel to muscle fiber direction).
c
One raw meat sample (measured parallel to muscle fiber direction) did not
completely fracture during the tensile tests and therefore stiffness could not be quan-
tified. This sample was omitted from the analyses, and sample size was reduced to nine.
increased approximately 47% in roasted yams, it decreased in roas-
ted beets and carrots. This difference leads to the prediction that
force per chew will actually be higher in roasted versus raw beets
and carrots. Such force increases may be mitigated, however, by
fewer chews overall because increased fragmentation occurs per
chew at lower (toughness/stiffness)0.5 (Agrawal et al., 1997). In other
words, foods with higher stiffness and relatively low toughness
undergo less deformation prior to fracture. Therefore, in the space-
limited environment between occluding teeth, these foods will
fracture more per chew. Increased fracture rates also explain why
foods of low (toughness/stiffness)0.5 are consumed with more
muscular effort per chew; as the teeth come into contact with the
food they require more force to propagate a larger number of frac-
tures within the material.
In addition to material property changes, cooking may also in-
crease the nutritional density of tubers and other underground
storage organs through dehydration, increasing digestibility, and
lowering cost of digestion (Carmody et al., 2011), all of which might
further reduce masticatory effort per calorie of food. While we
focused only on the inner, edible portion of the tubers, Dominy et al.
(2008) found that cooking also makes removal of the tough, outer
casing of tubers much easier. Improving the ability for hominins to
access the edible portion of underground storage organs would
have allowed for overall increases in net energy gained from the
food as less effort is required for ingestion.
Although the tuber data support the hypothesis that mechani-
cal and thermal processing techniques could have allowed for the
postcanine size decreases within Homo, the meat results are more
difficult to interpret. Contrary to predictions, mechanical tenderi-
zation did not affect meat toughness and roasted meat was actually
tougher and required approximately 50e220% more stress to
fracture than raw meat. Toughness changes, however, do not
necessarily mean that more masticatory effort must be expended
to chew raw versus roasted meat. As previously discussed, primate
molars are poorly adapted to chewing raw meat. Compression does
not produce fractures in raw meat, which instead must be sheared
or pulled (this is why cutting and tensile tests were used to mea-
sure meat properties.). For example, the meat used for this study
was hit 20 times with a replica Oldowan hammer stone and did not
163
fracture at all, but was instead simply mashed. Cooking, however,
may improve masticatory performance by increasing masticatory
efficiency. We calculated (toughness/stiffness)0.5 for the material
properties that primarily describe the meat connective tissue
(toughness and average stiffness measured parallel and perpen-
dicular to fiber direction, respectively) and the meat muscle fibers
(toughness and average stiffness measured perpendicular and
parallel to fiber direction, respectively) (Table 4). While the
(toughness/stiffness)0.5 of meat connective tissue changed only
slightly with roasting (~4% increase), it decreased nearly a third
(~31%) for the muscle fibers. Although a decrease in (toughness/
stiffness)0.5 predicts an increase in masticatory force per chew,
these increases may be mitigated by an increase in the rate at
which fractures are produced by the teeth (Agrawal et al., 1997,
reduction in the number of chews required, and therefore lower
overall masticatory effort (i.e., masticatory force per
chew  number of chews).
Another way in which cooking may have helped hominins
chew meat is that roasting stiffens meat parallel to fiber direc-
tion and decreases energy loss (hysteresis). Although fractures in
meat tend to run preferentially through the weaker perimysial
(connective tissue) bonds as opposed to breaking the tougher
muscle fibers (Purslow, 1985; Lewis and Purslow, 1990; Willems
and Purslow, 1997; Lillford, 2001), when muscle fiber fractures
do develop, comminution efficiency (food breakdown per chew)
will increase. The maximum number of particles possible from
connective tissue fracturing is positively correlated with the
number of muscle fibers present. In a given volume of food, fiber
number is greatest in slices running against the grain of the meat
and lowest in cuts following the longitudinal axis of the muscle.
In the latter case especially, stiffening with roasting may make
the food less ‘displacement limited’ and reduce fracture strain.
Although ultimate fracture strain was not different between raw
and roasted meat, there was a clear dip in stress at approxi-
mately 30% strain for the roasted meat pulled parallel to fiber
direction (Fig. 3). This dip did not occur in any of the other
curves and may indicate fracture initiation, breakage of the first
muscle fiber, after which the crack deviates into the weaker
perimysium and eventually moves across the remaining fibers
(increasing stress) to completely fracture the meat into two
pieces. A decrease in energy loss with roasting will further aid
fracture propagation and significantly increase the probability of
fracture in the limited strain environment between two
occluding teeth (Fig. 4, Table 3).
Finally, as with tubers, roasting may make the meat more
nutritionally dense, allowing for less consumption per calorie.
Water loss was significant with roasting, 35e40% by mass, greatly
increasing the amount of nutrients per gram. Digestive costs may
also improve with cooking as shown in studies of Burmese pythons
(Boback et al., 2007) and mice (Carmody et al., 2011) fed raw versus
cooked meat. Cooking also has the added benefit of reducing
endogenous parasites and killing bacteria that are especially
prevalent in meat (particularly scavenged meat; Ragir et al., 2000)
and which might cause illness. Reducing immune and digestive
costs will increase the net energy gained from roasted meat
(Carmody and Wrangham, 2009), and therefore less food would
need to be ingested to attain a certain number of calories.
In conclusion, the results of this study indicate a substantial
reduction in masticatory effort resulting from the use of simple
food processing techniques that were available to hominins, espe-
cially after the start of the Lower Paleolithic. Tubers and meat
responded differently to processing, however, which cautions
against grouping these (and other) foods together when discussing
the potential ramifications of food processing behavior for
164 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
mastication. It should also be noted that masticatory forces are
distributed across the occlusal surface of the tooth, and that dental
stress (force per area) is one of the main contributors to food
fracture. Eng et al. (2013) calculated maximum bite stress at the
second molar in apes and hominins, and found that although dental
stress remained fairly constant across most taxa (r2 ¼ 0.93), Homo
species fell well below the regression line, largely caused by a
substantial decrease in the amount of maximum bite force that
they could produce. This large residual suggests a grade shift with
the genus Homo in which the most mechanically demanding foods
that were consumed no longer required high dental stresses,
probably because of the use of food processing techniques to soften
the foods prior to consumption.
Regardless of the type of processing methods employed, it is
reasonable to predict that hominins would choose to processes
the foods that were the most mechanically demanding and
required the highest masticatory forces to consume. Therefore,
by processing foods, selection would no longer act to maintain
features necessary to generate high occlusal stresses or to
maintain energetically costly masticatory structures such as large
muscles and heavy, robust facial bones (Brace, 1967, 1995;
Wolpoff, 1971; Wrangham et al., 1999; Teaford et al., 2002;
Klein, 2009; Lieberman, 2011). This leaves open the possibility
for smaller postcanine teeth to evolve for other reasons, such as
to fit into shorter, less prognathic faces (for review, see
Lieberman, 2011).
Future research
The data presented in this study highlight the need to test the
effects of food processing on masticatory performance variables.
While material property tests are both useful and relatively inex-
pensive to perform on a wide variety of foods and processing types,
the relationship between food properties and fracture in the oral
cavity is complex. For example, the low toughness and high
(toughness/stiffness)0.5 of raw meat compared with both raw and
roasted tubers leads to the prediction of less force per chew when
consuming meat. Therefore, it is reasonable to hypothesize that the
addition of more raw meat to hominin diets could have made
possible the evolution of smaller, less robust masticatory
morphology in the genus Homo by relaxing selection on having
large, thickly-enameled teeth, as well as many features of the skull
that generate and withstand large masticatory forces. A caveat to
the material property data, however, is that the specific testing
environments used were conducive to fracture in meat (cutting and
tensing). As discussed previously, the ability of hominins to
comminute this food source efficiently in the raw state is ques-
tionable. As with chimpanzees, considerable chewing time and
effort may have been required to consume raw meat, and even
though the force per chew may have been low, many repetitive
chewing cycles would have been necessary (a hypothesis that re-
quires further testing).
Future research should also focus on testing the material
properties of other food and processing types relevant to early
hominins. Pounding and dry roasting over an open flame are only
two of many processing types that would have been available to
early hominins, and roasting was performed in this experiment
only to a single, relatively high, temperature. Many other methods
such as below-ground slow roasting, soaking, leaching, chemical
tenderization and especially slicing, grinding, and slow drying
over a small fire or in the hot sun may have been employed as
well. It is also important to note that these methods are not
mutually exclusive and multiple processing steps may have been
performed on foods. Additionally, processing techniques have
different effects on the material properties of different foods. For
example, although boiling greatly decreases potato and white
onion toughness, it has no effect on the toughness of white turnips
(Lucas, 2004). A number of factors such as the amount of starch
and fiber in plants, and age, fat reserves, amount and distribution
of connective tissue in muscle tissue will alter fracture properties.
Only four domesticated foods (three tubers and goat meat) were
tested and although they are representative of food sources
potentially important to early hominins, testing of additional
foods, especially wild vegetation and game meat will further
inform hominin dietary hypotheses.
Acknowledgments
We are very grateful to Rachel Carmody, Andrew Cunningham,
Carolyn Eng, Tanya Smith and Richard Wrangham for helpful dis-
cussion and comments. We would also like to thank two anony-
mous reviewers who helped to improve this manuscript. This work
was funded by the National Science Foundation through a doctoral
dissertation improvement grant (#0925688) awarded to K. Zink,
and also by the American School of Prehistoric Research (Peabody
Museum, Harvard University).
References
Agrawal, K.R., Lucas, P.W., Prinz, J.F., Bruce, I.C., 1997. Mechanical properties of foods
responsible for resisting food breakdown in the human mouth. Arch. Oral Biol.
42, 1e9.
Agrawal, K.R., Lucas, P.W., Bruce, I.C., Prinz, J.F., 1998. Food properties that influence
neuromuscular activity during human mastication. J. Dent. Res. 77, 1931e1938.
Alvarez, M.D., Canet, W., 2001. Kinetics of thermal softening of potato tissue heated
by different methods. Eur. Food Res. Technol. 212, 454e464.
Ashby, M.F., Jones, D.R.H., 1996. Engineering Materials 1: an Introduction to their
Properties and Applications, Second edition. Butterworth-Heinemann, Boston.
Atkins, A.G., Mai, Y.W., 1979. Guillotining of materials. J. Mat. Sci. 14, 2747e2754.
Baird, L., Rodwell, J., 2005. The Complete Book of Raw Food: Healthy, Delicious
Vegetarian Cuisine Made with Living Foods. Healthy Living Books/Hatherleigh
Press, New York.
Beleia, A., Yamashita, F., de Moraes, S.R., da Silveira, C.A., Miranda, L.A., 2004a.
Textural changes during cooking of cassava (Manihot esculenta Crantz) roots.
J. Sci. Food Agr. 84, 1975e1978.
Beleia, A., Prudencio-Ferreira, S.H., Yamashita, F., Sakamoto, T.M., Ito, L., 2004b.
Sensory and instrumental texture analysis of cassava (Manihot esculenta Crantz)
roots. J. Texture Stud. 35, 542e553.
Ben-Dor, M., Gopher, A., Hershkovitz, I., Barkai, R., 2011. Man the fat hunter: the
demise of Homo erectus and the emergence of a new hominin lineage in the
Middle Pleistocene (ca. 400 kyr) Levant. PLoS One 6.
Berna, F., Goldberg, P., Horwitz, L.K., Brink, J., Holt, S., Bamford, M., Chazan, M., 2012.
Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonder-
werk Cave, Northern Cape province, South Africa. Proc. Natl. Acad. Sci. 109,
E1215eE1220.
Binner, S., Jardine, W.G., Renard, C.M.C.G., Jarvis, M.C., 2000. Cell wall modifications
during cooking of potatoes and sweet potatoes. J. Sci. Food Agr. 80, 216e218.
Boback, S.M., Cox, C.L., Ott, B.D., Carmody, R., Wrangham, R.W., Secor, S.M., 2007.
Cooking and grinding reduces the cost of meat digestion. Comp. Biochem.
Physiol. A 148, 651e656.
Boesch, C., Boesch-Achermann, H., 2000. The Chimpanzees of the Taï Forest:
Behavioural Ecology and Evolution. Oxford University Press, New York.
Brace, C.L., 1967. Environment, tooth form, and size in the Pleistocene. J. Dent. Res.
46, 809e816.
Brace, C.L., 1995. Biocultural interaction and the mechanism of mosaic evolution in
the emergence of modern morphology. Am. Anthropol. 97, 711e721.
Bunn, H.T., 1981. Archaeological evidence for meat-eating by Plio-Pleistocene
hominids from Koobi Fora and Olduvai Gorge. Nature 291, 574e577.
Bunn, H.T., 1994. Early Pleistocene hominid foraging strategies along the ancestral
Omo river at Koobi-Fora, Kenya. J. Hum. Evol. 27, 247e266.
Bunn, H.T., 2007. Meat made us human. In: Ungar, P. (Ed.), Evolution of the Human
Diet: the Known, the Unknown, and the Unknowable. Oxford University Press,
New York, pp. 191e211.
Bunn, H.T., Kroll, E.M., 1986. Systematic butchery by Plio-Pleistocene hominids at
Olduvai-Gorge, Tanzania. Curr. Anthropol. 27, 431e452.
Carmody, R.N., Wrangham, R.W., 2009. The energetic significance of cooking.
J. Hum. Evol. 57, 379e391.
Carmody, R.N., Weintraub, G.S., Wrangham, R.W., 2011. Energetic consequences of
thermal and nonthermal food processing. Proc. Natl. Acad. Sci. 108,
19199e19203.
Chamberlain, A.T., Wood, B.A., 1985. A reappraisal of variation in hominid
mandibular corpus dimensions. Am. J. Phys. Anthropol. 66, 399e405.
 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
Chang, H.J., Wang, Q., Zhou, G.H., Xu, X.L., Li, C.B., 2010. Influence of weak organic
acids and sodium chloride marination on characteristics of connective tissue
collagen and textural properties of beef semitendinosus muscle. J. Texture Stud.
41, 279e301.
Christensen, M., Purslow, P.P., Larsen, L.M., 2000. The effect of cooking temperature
on mechanical properties of whole meat, single muscle fibres and perimysial
connective tissue. Meat Sci. 55, 301e307.
Christensen, M., Young, R.D., Lawson, M.A., Larsen, L.M., Purslow, P.P., 2003. Effect of
added m-calpain and post-mortem storage on the mechanical properties of
bovine single muscle fibres extended to fracture. Meat Sci. 66, 105e112.
Christensen, M., Larsen, L.M., Ertbjerg, P., Purslow, P.P., 2004. Effect of proteolytic
enzyme activity and heating on the mechanical properties of bovine single
muscle fibres. Meat Sci. 66, 361e369.
Combes, S., Lepetit, J., Darche, B., Lebas, F., 2003. Effect of cooking temperature and
cooking time on Warner-Bratzler tenderness measurement and collagen con-
tent in rabbit meat. Meat Sci. 66, 91e96.
Dan, H., Watanabe, H., Dan, I., Kohyama, K., 2003. Effects of textural changes in
cooked apples on the human bite, and instrumental changes. J. Texture Stud. 34,
499e514.
Darvell, B.W., Lee, P.K.D., Yuen, T.D.B., Lucas, P.W., 1996. A portable fracture
toughness tester for biological materials. Meas. Sci. Technol. 7, 954e962.
Dilek, M., Polat, H., Kezer, F., Korcan, E., 2011. Application of locust bean gum edible
coating to extend shelf life of sausages and garlic-flavored sausage. J. Food
Process. Pres. 35, 410e416.
Dixon, C.L., Woerner, D.R., Tokach, R.J., Chapman, P.L., Engle, T.E., Tatum, J.D.,
Belk, K.E., 2012. Quantifying the aging response and nutrient composition for
muscles of the beef round. J. Anim. Sci. 90, 996e1007.
Dominguez-Rodrigo, M., Barba, R., 2006. New estimates of tooth mark and per-
cussion mark frequencies at the FLK Zinj site: the carnivore-hominid-carnivore
hypothesis falsified. J. Hum. Evol. 50, 170e194.
Dominguez-Rodrigo, M., de la Torre, I., De Luque, L., Alcala, L., Mora, R.,
Serrallonga, J., Medina, V., 2002. The ST site complex at Peninj, West Lake
Natron, Tanzania: implications for early hominid behavioural models.
J. Archaeol. Sci. 29, 639e665.
Dominguez-Rodrigo, M., Pickering, T.R., Semaw, S., Rogers, M.J., 2005. Cutmarked
bones from Pliocene archaeological sites at Gona, Afar, Ethiopia: implications
for the function of the world's oldest stone tools. J. Hum. Evol. 48, 109e121.
Dominy, N.J., Vogel, E.R., Yeakel, J.D., Constantino, P., Lucas, P.W., 2008. Mechanical
properties of plant underground storage organs and implications for dietary
models of early hominins. Evol. Biol. 35, 159e175.
Duan, X., Zhang, M., Mujumdar, A.S., Wang, R., 2010. Trends in microwave-assisted
freeze drying of foods. Dry. Technol. 28, 444e453.
Eng, C.M., Lieberman, D.E., Zink, K.D., Peters, M.A., 2013. Bite force and occlusal
stress production in hominin evolution. Am. J. Phys. Anthropol. 151, 544e557.
Ennos, A.R., 2012. Solid Biomechanics. Princeton University Press, Princeton.
Finney, E.E., Hall, C.W., 1967. Elastic properties of potatoes. Trans. Am. Soc. Agr. Eng.
67, 4e8.
Gibson, L.J., Ashby, M.F., 1997. Cellular Solids: Structure and Properties, Second
edition. Cambridge University Press, New York.
Goh, S.M., Charalambides, M.N., Williams, J.G., 2005. Characterization of the
nonlinear viscoelastic constitutive properties of mild cheddar cheese from
indentation tests. J. Texture Stud. 36, 459e477.
Goodall, J., 1986. The Chimpanzees of Gombe: Patterns of Behaviour. Harvard
University Press, Massachusetts.
Goren-Inbar, N., Alperson, N., Kislev, M.E., Simchoni, O., Melamed, Y., Ben-Nun, A.,
Werker, E., 2004. Evidence of hominin control of fire at Gesher Benot Ya'aqov,
Israel. Science 304, 725e727.
Greve, C.L., McArdle, R.N., Gohlke, J.R., Labavitch, J.M., 1994a. Impact of heating on
carrot firmness: changes in cell wall components. J. Agric. Food Chem. 42,
2900e2906.
Greve, L.C., Shackel, K.A., Ahmadi, H., McArdle, R.N., Gohlke, J.R., Labavitch, J.M.,
1994b. Impact of heating on carrot firmness: contribution of cellular turgor.
J. Agric. Food Chem. 42, 2896e2899.
Hall, K.R.L., Schaller, G.B., 1964. Tool-using behavior of the California sea otter.
J. Mammal. 45, 287e298.
Hatley, T., Kappelman, J., 1980. Bears, pigs, and Plio-Pleistocene hominids: a case for
the exploitation of below ground food resources. Hum. Ecol 8, 371e387.
de Huidobro, F.R., Miguel, E., Blazquez, B., Onega, E., 2005. A comparison between
two methods (Warner-Bratzler and texture profile analysis) for testing either
raw meat or cooked meat. Meat Sci. 69, 527e536.
Keeley, L.H., Toth, N., 1981. Microwear polishes on early stone tools from Koobi-Fora,
Kenya. Nature 293, 464e465.
King, D.A., Dikeman, M.E., Wheeler, T.L., Kastner, C.L., Koohmaraie, M., 2003. Chilling
and cooking rate effects on some myofibrillar determinants of tenderness of
beef. J. Anim. Sci. 81, 1473e1481.
Klein, R.G., 2009. The Human Career: Human Biological and Cultural Origins, Third
edition. The University of Chicago Press, Chicago.
Laden, G., Wrangham, R., 2005. The rise of the hominids as an adaptive shift in
fallback foods: plant underground storage organs (USOs) and australopith or-
igins. J. Hum. Evol. 49, 482e498.
Lahr, M.M., Wright, R.V.S., 1996. The question of robusticity and the relationship
between cranial size and shape in Homo sapiens. J. Hum. Evol. 31, 157e191.
Lewis, G.J., Purslow, P.P., 1989. The strength and stiffness of perimysial connective-
tissue isolated from cooked beef muscle. Meat Sci. 26, 255e269.
165
Lewis, G.J., Purslow, P.P., 1990. Connective tissue differences in the strength of
cooked meat across the muscle fibre direction due to test specimen size. Meat
Sci. 28, 183e194.
Lieberman, D., 2011. The Evolution of the Human Head. Belknap Press of Harvard
University Press, Massachusetts.
Lillford, P.J., 2001. Mechanisms of fracture in foods. J. Texture Stud. 32, 397e417.
Loucks, L.J., Ray, E.E., Berry, B.W., Leighton, E.A., Gray, D.G., 1984. Effects of me-
chanical tenderization and cooking treatments upon product attributes of pre-
rigor and post-rigor beef roasts. J. Anim. Sci. 58, 626e630.
Lucas, P.W., 2004. Dental Functional Morphology: How Teeth Work. Cambridge
University Press, New York.
Lucas, P.W., Beta, T., Darvell, B.W., Dominy, N.J., Essackjee, H.C., Lee, P.K.D., Osorio, D.,
Ramsden, L., Yamashita, N., Yuen, T.D.B., 2001. Field kit to characterize physical,
chemical and spatial aspects of potential primate foods. Folia Primatol. 72,
11e25.
McHenry, H.M., 1994. Tempo and mode in human evolution. Proc. Natl. Acad. Sci. 91,
6780e6786.
McHenry, H.M., Coffing, K., 2000. Australopithecus to Homo: transformations in body
and mind. A. Rev. Anthropol. 29, 125e146.
McPherron, S.P., Alemseged, Z., Marean, C.W., Wynn, J.G., Reed, D., Geraads, D.,
Bobe, R., Bearat, H.A., 2010. Evidence for stone-tool-assisted consumption of
animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466,
857e860.
Milton, K., 1999. A hypothesis to explain the role of meat-eating in human evolu-
tion. Evol. Anthropol. 8, 11e21.
Mittal, G.S., Nadulski, R., Barbut, S., Negi, S.C., 1992. Textural profile analysis test
conditions for meat products. Food Res. Int. 25, 411e417.
Mutungi, G., Purslow, P., Warkup, C., 1995. Structural and mechanical changes in
raw and cooked single porcine muscle-fibers extended to fracture. Meat Sci. 40,
217e234.
Ng, A., Waldron, K.W., 1997. Effect of cooking and pre-cooking on cell-wall chem-
istry in relation to firmness of carrot tissues. J. Sci. Food Agr. 73, 503e512.
Oyen-Tiesma, M., Cook, R.F., 2001. Technique for estimating fracture resistance of
cultured neocartilage. J. Mat. Sci. Med. 12, 327e332.
Pietrasik, Z., Shand, P.J., 2005. Effects of mechanical treatments and moisture
enhancement on the processing characteristics and tenderness of beef semi-
membranosus roasts. Meat Sci. 71, 498e505.
Plummer, T., 2004. Flaked stones and old bones: biological and cultural evolution at
the dawn of technology. Am. J. Phys. Anthropol. S39, 118e164.
Pobiner, B.L., Rogers, M.J., Monahan, C.M., Harris, J.W., 2008. New evidence for
hominin carcass processing strategies at 1.5 Ma, Koobi Fora, Kenya. J. Hum. Evol.
55, 103e130.
Purslow, P.P., 1985. The physical basis of meat texture: observations on the fracture
behavior of cooked bovine M. semitendinosus. Meat Sci. 12, 39e60.
Purslow, P.P., 1991a. Notch-sensitivity of nonlinear materials. J. Mat. Sci. 26,
4468e4476.
Purslow, P.P., 1991b. Measuring meat texture and understanding its structural basis.
In: Vincent, J.F.V., Lillford, P.J. (Eds.), Feeding and the Texture of Food. Cambridge
University Press, Cambridge, pp. 35e56.
Ragir, S., 2000. Diet and food preparation: rethinking early hominid behavior. Evol.
Anthropol. 9, 153e155.
Ragir, S., Rosenberg, M., Tierno, P., 2000. Gut morphology and the avoidance of
carrion among chimpanzees, baboons, and early hominids. J. Anthropol. Res. 56,
477e512.
Roebroeks, W., Villa, P., 2011. On the earliest evidence for habitual use of fire in
Europe. Proc. Natl. Acad. Sci. 108, 5209e5214.
Semaw, S., Renne, P., Harris, J.W., Feibel, C.S., Bernor, R.L., Fesseha, N., Mowbray, K.,
1997. 2.5-million-year-old stone tools from Gona, Ethiopia. Nature 385,
333e336.
Semaw, S., Rogers, M.J., Quade, J., Renne, P.R., Butler, R.F., Dominguez-Rodrigo, M.,
Stout, D., Hart, W.S., Pickering, T., Simpson, S.W., 2003. 2.6-million-year-old
stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia.
J. Hum. Evol. 45, 169e177.
Sui, Z.Q., Lucas, P.W., Corke, H., 2006. Optimal cooking time of noodles related to
their notch sensitivity. J. Texture Stud. 37, 428e441.
Teaford, M.F., Ungar, P.S., Grine, F.E., 2002. Paleontological evidence for the diets of
African Plio-Pleistocene hominins with special reference to early Homo. In:
Ungar, P., Teaford, M. (Eds.), Human Diet: Its Origin and Evolution. Bergin and
Garvey, Connecticut, pp. 143e166.
Thiel, B.L., Donald, A.M., 2000. Microstructural failure mechanisms in cooked and
aged carrots. J. Texture Stud. 31, 437e455.
Tornberg, E., 2005. Effects of heat on meat proteins: implications on structure and
quality of meat products. Meat Sci. 70, 493e508.
Ungar, P.S., Grine, F.E., Teaford, M.F., 2006. Diet in early Homo: a review of the
evidence and a new model of adaptive versatility. A. Rev. Anthropol. 35,
209e228.
Van Loocke, M., Lyons, C.G., Simms, C.K., 2006. A validated model of passive muscle
in compression. J. Biomech. 39, 2999e3009.
Vincent, J.F.V., Jeronimidis, G., Khan, A.A., Luyten, H., 1991. The wedge fracture test: a
new method for measurement of food texture. J. Texture Stud. 22, 45e57.
Vogel, E.R., van Woerden, J.T., Lucas, P.W., Atmoko, S.S.U., van Schaik, C.P.,
Dominy, N.J., 2008. Functional ecology and evolution of hominoid molar enamel
thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. J. Hum.
Evol. 55, 60e74.
166 K.D. Zink et al. / Journal of Human Evolution 77 (2014) 155e166
Willems, M.E.T., Purslow, P.P., 1997. Mechanical and structural characteristics of
single muscle fibres and fibre groups from raw and cooked pork longissimus
muscle. Meat Sci. 46, 285e301.
Wolpoff, M.H., 1971. Metric Trends in Hominid Dental Evolution. Press of Case
Western Reserve University, Cleveland.
Wolpoff, M.H., 1973. Posterior tooth size, body size, and diet in South African gracile
australopithecines. Am. J. Phys. Anthropol. 39, 375e393.
Wood, B., Collard, M., 1999. The changing face of genus Homo. Evol. Anthropol. 8,
195e207.
Wrangham, R., 2007. The cooking enigma. In: Ungar, P. (Ed.), Evolution of the Hu-
man Diet: the Known, the Unknown, and the Unknowable. Oxford University
Press, New York, pp. 308e323.
Wrangham, R., Conklin-Brittain, N., 2003. 'Cooking as a biological trait'. Comp.
Biochem. Physiol. A 136, 35e46.
Wrangham, R.W., Jones, J.H., Laden, G., Pilbeam, D., Conklin-Brittain, N., 1999. The
raw and the stolen: cooking and the ecology of human origins. Curr. Anthropol.
40, 567e594.