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Taphonomic comparison of bone modifications caused by wild and captive

wolves (Canis lupus)

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DOI: 10.1016/j.quaint.2013.08.017

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 Quaternary International 330 (2014) 126e135

Contents lists available at ScienceDirect

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

Taphonomic comparison of bone modifications caused by wild and

captive wolves (Canis lupus)
Nohemi Sala a, *, Juan Luis Arsuaga a, Gary Haynes b
a
Departamento de Paleontología, Universidad Complutense de Madrid and Centro Mixto UCM-ISCIII de Evolución y Comportamiento Humanos, C/ Monforte
de Lemos 5, 28029 Madrid, Spain
b
Department of Anthropology, University of Nevada, Reno, USA

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

Article history: This work presents data obtained from experiments conducted on wild and captive wolves. Actualism is
Available online 30 August 2013 a very useful tool for taphonomic studies, as it allows us to understand the behavior of fauna in the past.
However, not many past experimental studies have dealt with wolves as taphonomic agents. The results
of the study show that wolves modify animal carcasses in advanced stages that include fracturing the
bones in order to consume the marrow. By comparing captive and wild wolves, we observe that captive
wolves often modify ungulate carcasses to a greater degree than do wild wolves. Moreover, factors such
as the size of the ungulate and the period of availability of the carcass influence the type and degree of
bone alteration. Tooth mark dimensions also allow us to compare wolves with other large carnivores and
reveal that wolves differ significantly from large felids and ursids, and they have more in common with
hyenids.
Ó 2013 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction wolves and carcasses. We present the first comparative study of

The wolf (Canis lupus) is a carnivore present in many Pleistocene
sites. The first appearance of C. lupus on the Iberian Peninsula was
found in the level TGIII of Trinchera Galería site (Sierra de Ata-
puerca) (García and Arsuaga, 1998) dated to ca. 450 ka by TL (Berger
et al., 2008) and ca. 250 ka by combined ESR-U/Th on teeth
(Falguères et al., 2013). Also, canids (Canis sp.) have been found in
the Middle Pleistocene deposits of the Sima de los Huesos and
Trinchera Dolina (TD10, TD11) (García and Arsuaga, 1999; García
García, 2003; Bischoff et al., 2007; García and Arsuaga, 2011).
Wolves are considered taphonomic agents in relation to the bone
modification in some Pleistocene sites (e.g. Castel, 2004; Stiner,
2004; Utrilla et al., 2010). There are some previous experimental
studies available that discuss wolves as taphonomic agents
(Haynes, 1980a, 1980b, 1981, 1982, 1983a, 1983b; Binford, 1981;
Nadal and Lorenzo, 1996; Fosse et al., 2004; Campmas and
Beauval, 2008; Esteban-Nadal et al., 2008, 2010; Yravedra et al.,
2011). However, these experimental studies usually refer separately
to carnivores held in captivity and carnivores in the wild. Addi-
tionally, previous studies took only a few experimental conditions
into account, such as ungulate size or duration of exposure between
* Corresponding author.
E-mail address: nsala@isciii.es (N. Sala).
bone modification caused by wild and captive wolves and we
control for several experimental conditions in order to better un-
derstand the behavior of this carnivore. The aim of this study is to
provide new data on bone modification patterns and tooth mark
dimensions caused by both wild and captive wolves.
2. Materials and methods
Experiments on captive wolves were carried out in the Cañada
Real Nature Center (Madrid, Spain), Carlos Avery Wildlife Man-
agement Area (Forest Lake, Minnesota, USA), and Wolf Park (Battle
Ground, Indiana, USA). Two established packs with 8e12 members
were maintained in each of two Carlos Avery half-acre fenced en-
closures, and one pack of about a dozen wolves were kept at a large
enclosure at Wolf Park. No other carnivores were ever allowed in
the enclosures. Wolves at Carlos Avery were given complete car-
casses of whitetail deer (Odocoileus virginianus) donated by hunters
or recovered from road kills, either fresh or frozen, without evis-
ceration or disarticulation. Haynes collected all bones in the two
enclosures in the summer of 1979, representing feedings over the
winter and spring 1978e79. The wolves at Wolf Park were given
carcass parts of donated livestock (horse, cattle, domesticated
camelids, pig), consisting of mainly articulated limbs with all skin
and flesh that had been refrigerated after sectioning or frozen. A

1040-6182/$ e see front matter Ó 2013 Elsevier Ltd and INQUA. All rights reserved.
http://dx.doi.org/10.1016/j.quaint.2013.08.017
 N. Sala et al. / Quaternary International 330 (2014) 126e135
sample of bones was collected from the enclosure in 1979. A wolf
pack with six members lives in Cañada Real Nature Center with a
well-established social hierarchy (Fig. 1). The experiments in
Cañada Real (labeled as CR) began in the winter of 2006 and were
completed in the summer of 2008. In the Cañada Real experiments,
the carcasses were eviscerated and were provided complete
without previous disarticulation. In all cases, wolves had access to
the intact carcasses, with no decay. Only wolves had access to the
carcasses.
Throughout the CR experiment, approximately 400 skeletal re-
mains were collected from ungulates of varying sizes and of
different exposure periods (Table 1). The duration of the experi-
ments conducted ranged from one day up to its maximum utili-
zation, when soft tissue and marrow are absolutely removed, which
could mean several years of exposure. Some of the carcasses were
monitored every day during consumption until all the bone re-
mains were removed (CR02 and CR03), with the exception of the
maximum utilization remains. Once we recovered the remains, all
were identified and cleaned.
The wild wolves studied in the USA and Canada were radio-
collared animals in free-roaming packs that were monitored daily
by wildlife researchers in the 1970s and 1980s. When packs in the
different study areas were seen killing or feeding upon fresh car-
casses of bison (Bison bison), moose (Alces alces), or whitetail deer,
researchers visited the sites after the wolves completed feeding, to
Fig. 1. Images of the wolf pack in the course of the experiment CR02. These pictures were taken on January 22, 2007, the date on which the experiment began.
127
record data and collect samples of bones. Some sites were also
visited by Haynes from one to seven years afterwards to collect
gnawed, broken, and weathered bones. Several thousand bones
and fragments from these studies were curated in the University of
Nevada, Reno’s Paleoenvironmental Laboratory, and many even-
tually will be deposited in the Smithsonian Institution’s National
Taphonomic Collection.
Experiments have been conducted on different types of prey in
terms of taxa, age and body size to establish these factors’ impact
on changes in the use of carcasses (Table 1).
The body size was established in base on weight and age of the
ungulates (Bunn, 1986). In this work we consider: i) Small sized un-
gulate (SSU) to adult specimens of Sus, Capra and Ovis genera and
juvenile specimens of Cervus and Odocoileus; ii) Medium sized un-
gulate (MSU) to adult specimens of Cervus and Odocoileus and juve-
nile specimens of equids iii) Large ungulates (LSU) to adult specimens
of Bos, Bison, Alces and Equus genera. The classification of bone type
includes: long bone (femur, tibia, humerus, radius, ulna) and flat
bone (skull, mandible, scapula, ribs, vertebra and innominate).
A total of 687 bone remains were recovered to study bone sur-
face modification (Table 1). A Nikon SMZ800 (stereoscopic zoom
microscope) was used to examine surface modification on bone
remains.
Carnivore damage was examined according to five stages of
consumption (from light to heavy: I, II, III, IV and V), specific to each
128 N. Sala et al. / Quaternary International 330 (2014) 126e135

Table 1
Inventory of carcasses analyzed. Number NR: number of specimens recovered after consumption.

Experiment Carcass Carcass age Ungulate size Time NR Total

Captive CR01 Sus scrofa A SSU 26 days 26 616

CR02 Cervus elaphus I SSU 1e4 days 22
CR03 Capra hircus A SSU 12 days 44
CR04.1 Bos taurus A LSU 12
CR04.2 Cervidae A MSU ME 11
CR04.3 Ovis aries A SSU ME 49
CR04.4 Sus scrofa A SSU ME 14
CR04.5 Indet. A e ME 125
CR07 Several taxa e e ME 94
WOPA Bos taurus A LSU Few dayse2 weeks 11
Bos taurus I MSU 2 weeks 5
Equus caballus A LSU 2 weeks 4
Equus caballus I MSU 2 weeks 2
Odocoileus virginianus A MSU ME 168
Odocoileus virginianus I SSU ME 27
Sus scrofa A SSU 2 weeks 2
Wild Isle Royale National Alces alces A MSU 3.5e5 months 6 71
Park (USA)
Wood Buffalo National Bison bison A LSU 2 weeks to ME 28
Park (Canada) Bison bison I MSU 2e3 weeks 13
Superior National Odocoileus virginianus A MSU Few days 10
Forest (USA) Odocoileus virginianus I MSU Few days 14
Total 687

I ¼ Immature; A ¼ Adult; ME ¼ Maximum exploitation; LSU ¼ Large sized ungulate; MSU ¼ Medium sized ungulate; SSU ¼ Small sized ungulate.

bone type, following the guidelines described by Haynes (1981,
1982). The revision of the Haynes method is based on the exclu-
sion of the soft tissue modification in order to compare the results
with archaeological assemblages where no meat is conserved (Sala,
2012) (Table 2). The stages have been tested by daily monitoring
carcass CR-02 and CR-03 with Cañada Real wolves.
Tooth marks on bone surfaces were classified into pits, punc-
tures, furrowing and scores (Maguire et al., 1980; Binford, 1981;
Haynes, 1980a, 1980b, 1983b). Tooth-mark distribution on bone
portions was recorded, considering three areas to take into account
the various bone densities based on their resistance to tooth
penetration: spongy or cancellous, thinning cortical and cortical

Table 2
Definition of bone modification stages, modified from Haynes (1980a, 1980b, 1981).

Low modification Moderate modification Heavy modification

I II III IV V

Skull Scores in horns Nasal bones and horns Nasal bones ragged at ends. e e
tooth scratched Premaxillaries broken
Maxillar Maxilla articulated. Preserves Isolated maxilla. It can Complete molar serie but Incomplete molar serie Isolated teeth
molar serie. Crenulated edges conserve alveolar process with a little bone associated
and/or perforations and the palate parcial or
totally. Punctures
Mandibles Complete hemimandible. Mandibular corpus and Complete molar serie but Incomplete molar serie. Isolated teeth
Furrowing in the angular diastema broken with a little bone associated
process and/or symphysis
Scapula Furrowing in the vertebral Vertebral border broken Scapular body broken. Furrowing in the glenoid Isolated fragment
border with sawtoothed edges Furrowing un the scapular articulation
spine
Humerus Greater tuberosities furrowed Tuberosities gone. Proximal epiphisis gone. About 1/3 shaft gone. Shaft cylinder or isolated
Furrowing in the head Distal epiphisis intact Furrowing in the distal shaft fragment
condyles
Radius Furrowing in distal end Distal end gone Furrowing in proximal Shaft cylinder Isolated fragment
epiphysis
Ulna Furrowing in olecranon process Olecranon process gone Desarticulated of radii Shaft fragment e
Pelvis Iliac crest and ischial tuberosity Scooping out of cancellous Ilium and ischium totally Fragment e
furrowed. Cancellous tissue tissue of ilium and ischium gone. Only acetabulum
exposed remains
Femur Furrowing in great trochanter. Furrowing in medial and Great trochanter gone Distal epyphisis gone. Shaft cylinder or isolated
Scores in femur head lateral condyles Femur head nearly gone fragment
Tibia Furrowing in proximal lateral Tibial tuberosity gone Furrowing in proximal Proximal epiphysis gone. Shaft broken, only distal
border medial border Distal end intact end remains
Metapodial Complete. Scores on the shaft Distal end gone Proximal end furrowed Shaft cylinder Isolated shaft fragment
and pitting on the distal
epiphysis
Talus Scores, pitting and furrowing Fractured e e e
Calcaneus Furrowing in calcaneal tuber Punctures in lateral surface Furrowing in articular Fragment e
surfaces
Phalanges Scores and pitting Furrowed Fractured Stomach dissolution e
evidences
 N. Sala et al. / Quaternary International 330 (2014) 126e135 129

bone (Selvaggio and Wilder, 2001; Domínguez-Rodrigo and
Piqueras, 2003; Delaney-Rivera et al., 2009). The length and
breadth of marks was measured using standard digital calipers
(sylvac) with an error of 0.01 mm (Fig. 2).
Metric data were compared to other experimental data (Sala,
2012; Delaney-Rivera et al., 2009; Domínguez-Rodrigo and Pique-
ras, 2003; Campmas and Beauval, 2008; Andrés et al., 2012; Saladié
et al., 2013) obtained from other living carnivores (Panthera leo,
Ursus arctos, Crocuta crocuta, Vulpes vulpes, Puma concolor and Pan-
thera onca). In order to make this metrical comparison, the location
of tooth marks on dense and spongy bone or cortical bone was
considered due to the impact of bone density on mark size (Delaney-
Rivera et al., 2009). Nevertheless, previous studies show that tooth
pit length on shafts is the best indicator of the responsible carnivore
taxa (Andrés et al., 2012; Sala, 2012). A 95% confidence interval was
than half in at least a portion of the bone length and 3: complete
circumference in at least a portion of the bone length).
3. Results
3.1. Bone modification patterns
Tables 3 and 4 show the number and frequency of tooth marks,
taking into account the size of the ungulate, the different bone type
(e.g. long and flat bone) and bone regions (cortical, thin cortical and
spongy bone tissue) comparing the sample consumed by wolves in
the wild and in captivity.
Table 3
Presence/absence of tooth marks in the bones analyzed.

used to compare the mean of tooth pits (length cortical). Wild wolves Captive wolves
For the univariate analysis, we performed a Kruskal Wallis test LSU MSU SSU LSU MSU SSU
to compare the differences between the wolves and the other living
Long bones 22/2 8/5 5/4 35/2 117/23 70/2
carnivore samples (Sala, 2012). When a significant difference
Flat bones 8/1 8/3 4/1 37/4 51/88 50/30
(p < 0.05) was found, we performed a Mann Whitney test (Mann
and Whitney, 1947) among all possible pairs of samples to deter-
mine which pairs differed significantly. Fracture patterns were In general terms, the bone modification in carcasses of varying
analyzed according to criteria developed by Villa and Mahieu sizes caused by wild and captive wolves is very intense. In per-
(1991), Bunn (1982, 1983), Haynes (1983a) and Lyman (1993, centage terms, the frequency of marked bones is higher in the
1994). This method analyzes the fracture location following captive wolves’ data than in the data collected from those in the
Lyman (1993, 1994); the fracture outline (longitudinal, transverse wild (Tables 3 and 4). The most common types of alteration pro-
and oblique); the angle formed by the fracture surface and the duced by wolves are pits and scores (Fig. 3), especially in the long
bone’s cortical surface (oblique, right or mixed); the characteristics bones diaphysis. However, furrowing with pitting and punctures
of the fracture edges (jagged or smooth); shaft fragment length (1: are common on long bone epiphyses. In the flat bones, the tooth
shafts that are less than one-fourth the original length; 2: length marks are generally most abundant in the cortical bone because the
between one-fourth and one-half; 3: between one-half and three- spongy bone is almost entirely consumed.
fourths; 4: more than three-fourths, essentially a complete or We also examined the bone modification patterns for each of
almost complete shaft); and shaft circumference (1: bone circum- the anatomical regions. As shown in Fig. 4 and Table 5, the bone
ference is less than half of the original; 2: circumference is more alteration patterns in long bones show higher degrees of

Fig. 2. Examples of SEM images of tooth marks (a: scores; b: punctures and ced: pits) showing the measurements considered in this study.
130 N. Sala et al. / Quaternary International 330 (2014) 126e135

Table 4

NR

3
5
1

2
20
14
13
1
12
Tooth mark frequencies in the study assemblage according to bone region.

e
e
Wild wolves

45.2
Large sized ungulates (LSU)

15
e
e
e
e
V

6
4
0
3
Long bones (N ¼ 24) Flat bones (N ¼ 9)

22.2

35.5
Proximal Ep Diaph Distal Ep Cortical Cancellous

IV

e
e
1
1
0

2
4
8
6
1
1
Pits 3 (12.5%) 5 (20.8%) 5 (20.8%) 2 (22.2%) 4 (44.4%)
Scores 4 (16.7%) 13 (54.2%) 4 (16.7%) 4 (44.4%) 4 (44.4%)

22.2

8.06
Punctures 4 (16.7%) 0 2 (8.3%) 0 2 (22.2%)

III

e
e
2

0
1
0
1
0
3
Furrowing 12 (50.0%) 1 (4.2%) 3 (12.5%) 1 (11.1%) 3 (33.3%)

Medium sized ungulates (MSU)

3.23
Long bones (N ¼ 13) Flat bones (N ¼ 10)

e
e
II

0
0
0
1
0
1
Small sized ungulates
Proximal Ep Diaph Distal Ep Cortical Cancellous

22.2

8.06
Pits 0 6 (46.1%) 0 3 (30.0%) 3 (30.0%)

e
e
0
1
1

0
0
0
1
0
4
Scores 0 4 (30.8%) 0 1 (10.0%) 3 (30.0%)

I
Punctures 0 0 0 0 1 (10.0%)
Furrowing 1 (7.7%) 0 0 4 (40.0%) 3 (30.0%)

NULL
Small sized ungulates (SSU)

e
e
0

0
0
0
0
0
0
0
Long bones (N ¼ 9) Flat bones (N ¼ 5)

NR

1
5
2
1

16
20
17
22
4
18
Proximal Ep Diaph Distal Ep Cortical Cancellous

e
Pits 0 0 0 1 (20.0%) 0
Scores 0 3 (33.3%) 1 (11.1%) 1 (20.0%) 0

22.2

30.9
13
e
Punctures 1 (11.1%) 1 (11.1%) 0 0 0

2
0
0

6
1
0
4
-
Furrowing 0 0 0 0 3 (60.0%)

Captive wolves

33.3

29.9
IV

e
2
1
0

9
4
8
5
1
2
-
Large sized ungulates (LSU)

Long bones (N ¼ 37) Flat bones (N ¼ 41)

22.2

14.4
III

e
Proximal Ep Diaph Distal Ep Cortical Cancellous

1
1
0

0
1
2
4
1
6
Pits 2 (5.4%) 28 (75.7%) 12 (32.4%) 2 (4.9%) 0

20.6
Scores 4 (10.8%) 28 (75.7%) 9 (24.3%) 1 (2.4%) 1 (2.4%)
Medium sized ungulates

12
e

e
Punctures 0 0 1 (2.7%) 1 (2.4%) 0
II

0
0
0

0
2
1

1
4
Furrowing 6 (16.2%) 5 (13.5%) 9 (24.3%) 0 2 (4.9%)

11.1

3.09
Medium sized ungulates (MSU)
e

e
0
0
1

1
0
0
0
0
2
I

Long bones (N ¼ 140) Flat bones (N ¼ 139)

Proximal Ep Diaph Distal Ep Cortical Cancellous

NULL

1.03
Pits 4 (2.9%) 99 (70.7%) 9 (6.4%) 9 (6.5%) 2 (1.4%)
e

e
0
0
0

0
0
0
0
1
0
Scores 1 (0.7%) 77 (55.0%) 4 (2.9%) 24 (17.3%) 2 (1.4%)
Quantitative data of the bone modification stage in long bones consumed by wolves.

Punctures 4 (2.9%) 7 (5.0%) 3 (2.1%) 20 (14.4%) 1 (0.7%)

NR

Furrowing 14 (10.0%) 39 (27.9%) 9 (6.4%) 8 (5.8%) 24 (17.3%)

e
6
5
8

7
7
9
4
1
1
Small sized ungulates (SSU) 27.6

Long bones (N ¼ 72) Flat bones (N ¼ 80)

e

e
V

0
0
0

0
0

0
3
2
3

Proximal Ep Diaph Distal Ep Cortical Cancellous

Pits 2 (2.8%) 65 (90.3%) 11 (15.3%) 38 (47.5%) 0

23.8

51.7
IV

Scores 3 (4.2%) 55 (76.4%) 6 (8.3%) 20 (25.0%) 4 (5.0%)

e
1
1
3

6
4
5
0
0
0

Punctures 1 (1.4%) 3 (4.2%) 3 (4.2%) 16 (20.0%) 3 (3.7%)

Furrowing 3 (4.2%) 16 (22.2%) 13 (18.1%) 14 (17.5%) 13 (16.2%)
33.3

17.2
III

Ep: epiphysis; Diaph: Diaphysis.

e
3
1
3

0
0
2
1
1
1

destruction when comparing captive wolves to wolves in the wild.

23.8

6.9
e
II

In other words, the wolves in captivity inflict more pronounced

2
2
1

2
0
0
0
0
0
Large sized ungulates

bone changes than those who are not confined.

14.3
e
0
0
1

0
0
0
0
0
0
0
I

3.2. Metric analysis

NULL

4.76

Table 6 provides a summary of statistics regarding tooth mark

e
0
1
0

0
0
0
0
0
0
0

dimensions. Andrés et al. (2012) provide the metrical data of wild

Captive wolves

wolves tooth marks from the collection published previously by

Wild wolves

Metapodial

Yravedra et al. (2011). Campmas and Beauval (2008) offer metrical

Humerus

Humerus

data of tooth marks caused by captive carnivores. Comparing our

Radius

Radius
Femur

Femur
Table 5

Tibia

Tibia
Ulna

Ulna

data with those obtained by these authors (Fig. 5), our sample is
%

closer to the Andrés et al. (2012) than the Campmas and Beauval
 N. Sala et al. / Quaternary International 330 (2014) 126e135 131

Fig. 3. Examples of bone modification caused by wolves.

(2008) data and, in some cases, our sample falls inside the range of
variation of the other two samples (e.g. length cortical).
When comparing the wolf metric data with data obtained from
other living carnivores (P. leo, U. arctos, C. crocuta, Panthera tigris,
P. onca and Puma concolor), almost all of which are present in
Pleistocene sites, there are statistical differences in the metric
characteristics of tooth marks between C. lupus and larger carni-
vores, such as lions or bears, but not between wolves and hyaenids
(Fig. 5 and Table 7).
3.3. Fracture pattern
Of the total number of bones analyzed, 85% exhibited fractures,
57.7% of the bones had tooth marks associated with fractures, and
90% of the long bones are fractured, taking into account all sizes of
ungulates. However, in this study, captive wolves fractured bones
more frequently than wild wolves (Fig. 6).
The fracture properties analysis (Table 8) indicates that there is
no dominant orientation of fractures. The data indicate that the
great majority (between 80.39% and 98.81%) of the broken bones
caused by wolves are characterized by obtuse or acute edge angles.
These data corroborate the typical fresh bone breakage demon-
strated by Villa and Mahieu (1991).
With regard to long bone fracturing, Fig. 7 and Table 8 shows the
relationship between the shaft circumference and shaft fragment
taking into account the ungulate sizes. More than 53% of large
ungulates have fracturing with the complete circumference of shaft
preserved while 32.5% are shaft fragments under three-quarters of
132 N. Sala et al. / Quaternary International 330 (2014) 126e135

Table 6
Descriptive statistics for measurements of pits, punctures and scores. The data displayed in the table show length and breadth (n: number of cases; Max: maximum value; Min:
minimum value; C.I.: Confidence Interval for mean and SD.: Standard Deviation; CV: variation coefficient).

n Mean Minimum Maximum St. Desv. IC  95% IC þ 95% CV

Punctures Length Cancellous 60 4.35 1.81 6.65 1.04 4.08 4.62 23.98
Thin cortical 70 3.90 1.95 7.41 1.10 3.64 4.16 28.11
Cortical 21 3.56 1.56 6.86 1.24 3.00 4.12 34.73
Breadth Cancellous 50 3.34 1.79 5.53 0.93 3.07 3.60 27.79
Thin cortical 38 3.12 1.02 6.12 1.19 2.73 3.51 38.11
Cortical 6 2.73 1.75 4.77 1.13 1.55 3.92 41.37
Pits Length Cancellous 54 2.81 1.24 4.45 0.68 2.62 2.99 24.21
Thin cortical 89 2.70 0.76 4.47 0.80 2.54 2.87 29.48
Cortical 218 2.11 0.82 3.70 0.64 2.02 2.19 30.22
Breadth Cancellous 37 2.31 1.23 3.90 0.59 2.11 2.50 25.34
Thin cortical 80 2.08 1.10 3.29 0.51 1.97 2.19 24.47
Cortical 151 1.65 0.66 3.07 0.53 1.56 1.73 32.08
Scores Breadth Cancellous 33 2.35 0.80 7.41 1.38 1.86 2.84 58.82
Thin cortical 53 1.07 0.50 2.24 0.36 0.98 1.17 33.06
Cortical 161 1.29 0.40 10.90 0.87 1.15 1.42 67.94

Fig. 4. Histograms showing the bone modification stage in long bones consumed by wolves.

Fig. 5. Mean values and 95% confidence intervals of tooth pit length on dense shafts of wolves (left) and other taxa (from left to right: bear, lion, hyena, fox and jaguar). In red is
represented Mean  1SD. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
 N. Sala et al. / Quaternary International 330 (2014) 126e135 133

Table 7
Results of the Mann Whitney U-tests for differences between the mean dimensions of wolf tooth marks in our sample and those from experimental data from other living
carnivores.

Cortical bone Cancellous bone

Length (n ¼ 274) Breadth (n ¼ 274) Length (n ¼ 86) Breadth (n ¼ 86)

n U value p n U value p n U value p n U value p

U. arctos 15 508.500 0.000 15 674.500 0.000 22 615.000 0.012 22 543.000 0.002

P. leo 134 5461.500 0.000 134 7399.000 0.000 56 1108.500 0.000 56 1275.500 0.000
P. tigris 73 2278.000 0.000 73 3739.500 0.000 82 1763.500 0.000 82 2399.500 0.000
P. onca 21 1471.500 0.000 20 1666.000 0.000 16 594.000 0.387 14 535.500 0.509
P. concolor 42 3754.000 0.000 10 1033.500 0.187 22 864.000 0.532 10 267.000 0.051
C. familiaris 42 1222.000 0.000 e e e 15 160.500 0.000 e e e
C. crocuta 213 27372.000 0.240 16 381.000 0.000 35 932.000 0.001 e e e

Values in bold are significant at p < 0.05.

Table 8 bones. Pits and scores are the most abundant types of tooth marks
Fracture properties in the bones broken by wolves according to criteria developed by we observed. These observations are consistent with those of other
Villa and Mahieu (1991), Bunn (1982, 1983), Haynes (1983a) and Lyman (1993, 1994).
LSU: Large Ungulate; MSU: Medium sized Ungulate; SSU: Small sized ungulate. *
authors (Binford, 1981; Haynes, 1982; Yravedra et al., 2011). The
Only long bones spongy tissue has been completely removed or consumed in large
parts of the sample.
LSU MSU SSU
The high frequency of tooth marked bones, especially in broken
Fracture outline Longitudinal 39.42 46.72 33.06 large ungulates bones, could be due to the mastication force; the
Transversal 38.69 39.90 33.06
wolf does not have as much mastication power as other large car-
Curved 21.90 13.38 33.87
Fracture angle Oblique 80.39 94.55 98.81 nivores, such as bears, hyenas or lions (Christiansen and Adolfssen,
Right 6.86 1.56 1.19 2005). This fact may explain why wolves need further processing to
Mixed 12.75 3.89 0.00 produce bone fracturing and the resulting frequencies of tooth
Edges Smooth 27.27 30.03 35.94
marked bones are very high.
Jagged 26.67 34.99 26.56
Crenulated 30.30 18.37 21.09
After wolves consume their prey, the bones of all skeletal re-
Shaft circumferencea <1/2 31.91 36.55 17.78 gions, especially from small and large ungulates, often display
>1/2 14.89 6.21 20.00 heavy modification. These data are consistent with previous studies
Complete 53.19 57.24 62.22 conducted on wolves (Binford, 1981; Haynes, 1982, 1983b; Nadal
Shaft fragmenta <1/4 26.19 41.38 26.09
and Lorenzo, 1996).
1/4e1/2 21.43 28.28 41.30
1/2e3/4 23.81 22.07 21.74 The results from the present study indicate presumable differ-
>3/4 28.57 8.28 10.87 ences between captive and wild wolves’ bone modifications.
LSU: Large sized ungulate; MSU: Medium sized ungulate; SSU: Small sized ungulate.
However, we must take into account some limitations of the pre-
a
Only long bones. sent study. The two samples (wild vs captive wolves) do not have
exactly the same sizes and same taxa of ungulate prey. Therefore, it
is not self-evident if the bones affected by wild wolves are less
the total length (Fig. 7). In medium sized ungulates, the proportion modified because of environmental conditions (captivity versus
of small splinters increases and the full circumference diaphysis free-roaming ability) or because carcasses affected by the wild
decreases (Fig. 7). wolves were generally larger and harder to modify. Comparing our
results with those obtained by other authors who have studied wild
4. Discussion wolves, advanced modification stages were only documented
either in small carcasses or juvenile carcasses from medium sized
Wolves generally tend to create numerous tooth marks when animals (Yravedra et al., 2011). Another study (Fosse et al., 2011)
consuming prey, especially on the cortical areas of long and flat carried out with wild wolves in Pologne show that medium sized

Fig. 6. Comparative histogram showing the fracture frequency in bones consumed by captive and wild wolves.
134 N. Sala et al. / Quaternary International 330 (2014) 126e135
Fig. 7. Three-dimensional bar diagrams showing relative frequencies of shaft length by shaft circumference in large size (left image) and medium size ungulates (right image). Shaft
length categories are: 1: <1/4 of the original length; 2: 1/4 to 1/2; 3: 1/2 to 3/4 and 4: >3/4 or complete. Shaft circumference categories are: 1: bone circumference is less than half
of the original; 2: circumference is more than half, and 3: complete circumference in at least a portion of the bone length.
ungulates (Cervus elaphus) recovered in kill sites display less bone
modification than our sample, such as with fracturing. These data
support the suggestion that captive carnivores inflict more bone
damage than conspecific wild counterparts. Those observations
were already perceived by Sala and Arsuaga (2013) in bear activity
and by Gidna et al. (2013) and Pobiner (2007) through experiments
conducted on lions. Other authors have also found more bone
damage inflicted by captive vs wild carnivores. It is possible that the
captive carnivores suffer from boredom and that they continue
gnawing due to this, causing more tooth-marking and bone damage
in contrast with wild animals (Haynes, 1982; Sala and Arsuaga,
2013). Nevertheless, further research regarding the wild wolf
sample is requiring for confirmation.
The results show that wolves have a significant ability to frac-
ture bones of ungulates of all sizes to obtain marrow. This ability
has usually been attributed solely to hyenas (Sutcliffe, 1970;
Maguire et al., 1980; Brain, 1981; Blumenschine, 1986; Marean
and Spencer, 1991; Marean et al., 1992; Pokines and Peterhans,
2007). The abundant bone fractures observed with a high per-
centage of bone splinters is consistent with data from other authors
(Binford, 1981; Haynes, 1982, 1983b; Nadal and Lorenzo, 1996).
Some of these bone fragments were recovered in the faeces
analyzed, indicating that wolves are able to swallow relatively large
amounts of bone fragments, which was also demonstrated by
Esteban-Nadal et al. (2010).
Canids usually are not regarded as taphonomical agents likely to
have made significant contributions to paleontological sites. This
may due to the lack of clear evidence in modern studies that wolves
generate bone accumulations like those in prehistoric sites (Joslin,
1967; Mech, 1970; Fox, 1971), and for this reason there is
disagreement over the role of canids as bone accumulating agents
in the past (Domínguez Rodrigo, 1994; Yravedra et al., 2011).
However, canids can become major taphonomic agents (through
secondary access to carcasses) in relation to modification of bone
assemblages (Díez, 1993; Huguet et al., 2001). Although the bone
accumulations in Pleistocene sites may not have been originally
created by wolves, they could have been major bone modifiers in
archaeological and paleontological sites.
5. Conclusions
Wolves modify animal carcasses in advanced stages that include
fracturing the bones in order to consume the marrow. Through
comparing captive and wild wolves, captive wolves often modify
bones from ungulate carcasses to a greater degree than wild
wolves. Moreover, factors such as size of ungulate and the period of
carcass availability influence the type and degree of bone alteration.
Those factors must be taken into account by other researchers in
order to reach a better understanding of carnivores as taphonomic
agents in the past. The results of this study show that caution is
needed with the results obtained from captive carnivores, and
more experimental data with wild carnivores and all sizes of un-
gulate prey are necessary.
When comparing the metric data from wolves with data ob-
tained from other living carnivores (P. leo, U. arctos, C. crocuta,
P. tigris, P. onca and P. concolor), almost all of which are present in
Pleistocene sites, there are statistical differences in the metric
characteristics of tooth marks between C. lupus and larger carni-
vores, such as lions or bears, but not between wolves and hyaenids.
The data gathered are of great importance when interpreting
paleontological and archaeological sites where the wolf is a likely
taphonomic agent.
Acknowledgments
The research was funded by the MICINN project GL2012-38434-
C03-01 and Ministerio de Educación (FPU grant AP2006-04737).
Thanks to Fundación Ancestros. Fieldwork with wild and captive
wolves in the USA and Canada was supported by a grant from the
US National Science Foundation, and to our colleagues at the Centro
Mixto UCM-ISCIII de Evolución y Comportamiento Humano. Thanks
to the staff of Cañada Real (Pelalejo, Madrid) and especially Pepe
España for allowing work with captive wolves. We are indebted to
many people that have allowed us access to important skeletal
collections under their care and kindly provided their help,
particularly Curtis Marean and Mary Stiner. Thanks also to the BBP
group and Chrissina Burke for their support and discussions.
Thanks to Lauren Ames and Mario Alcolea for the English revision
of the manuscript. We appreciate the many helpful comments and
suggestions provided by the three reviewers (Manuel Domínguez
Rodrigo, Philippe Fosse and other anonymous reviewer) that
improved the manuscript. Finally thanks to the editorial team,
especially to Ana Belén Marín Arroyo and Norm Catto.
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