Journal of Mammalogy, 97(4):1111–1124, 2016

DOI:10.1093/jmammal/gyw058
Published online March 31, 2016

A standardized framework for examination of oral lesions in wolf

skulls (Carnivora: Canidae: Canis lupus)
Luc Janssens,* Leen Verhaert, Daniel Berkowic, and Dominique Adriaens
Clinic for Orthopedic Surgery of Companion Animals, Hertstraat 50, 9000 Ghent, Belgium (LJ)
Clinic for Small Animal Dentistry, Lintsesteenweg 5, 2570 Duffel, Belgium (LV)
Natural History Collections, Department of Zoology, University of Ramat Aviv, Tel Aviv 69978, Israel (DB)
Department of Biology, Ghent University, Evolutionary Morphology of Vertebrates & Zoology Museum, K.L. Ledeganckstraat 35,

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9000 Ghent, Belgium (DA)
* Correspondent: coati1@icloud.com

Oral lesions in wolves (Carnivora: Canidae: Canis lupus) are usually reported in a nonstandardized manner, and
often only a few abnormalities are indicated. This approach has likely led to underreporting of oral lesions, thus
limiting our ability to interpret wolf health conditions and thus making comparisons across geographical and
taxonomic groups difficult. Here, we present a standardized oral exam protocol to examine wolf skulls for their
oral lesions. Using this protocol, we analyzed 40 skulls of adult wild Middle East wolves representing 1,680
teeth. Six wolves were Canis lupus arabs, 34 were Canis lupus pallipes. Only 3 skulls showed no oral lesions.
We were able to identify a large range of oral lesions and refined subclasses, exceeding the variety of what has
been reported on wolf oral lesions so far. No statistical differences were found in the type and number of lesions
between the 2 subspecies of wolves. Therefore, the lesions were pooled in subsequent analyses. This standardized
protocol should provide a useful framework to assess oral lesions in wolf skulls, facilitating rigorous comparisons
across geographic and taxonomic groups.

Key words: Canidae, Canis lupus arabs, Canis lupus pallipes, Carnivora, dental lesions, oral, oral lesions, periodontal disease, skull
lesions, wolf

© 2016 American Society of Mammalogists, www.mammalogy.org

The Middle East wolf is represented by 2 subspecies: Canis
lupus pallipes and Canis lupus arabs (Pocock 1935, 1939).
C. l. pallipes has a range that extends from India in the West,
to Palestine, the northern parts of Israel, and the Mediterranean
coast in the east (Pocock 1935, 1939; Mendelssohn 1982).
C. l. arabs is present in the desert areas of the southern parts
of Israel, below of the 50 mm isohyet (e.g., Negev Desert and
Arava Valley—Mendelssohn 1982), in the Egyptian Sinai
Desert, and the Arabian Peninsula. Populations of Middle
East wolves have declined considerably over the last decades
(Mendelssohn 1982). They are protected in Israel since 1954
and more recently in Oman but not in other countries where
they are considered a pest and hunted intensely (Ginsberg and
Macdonald 1990; Hefner and Geffen 1999). Although wolves
as a whole are considered to be “Least Concern” by the IUCN,
the Middle East population is thought to be in need of protec-
tion (Ginsberg and Macdonald 1990). Middle East wolves feed
on wildlife (hares, ibex, gazelles), livestock (chickens, sheep,
goats), berries and plants, and human garbage (Hefner and
Geffen 1999).
Severe oral abnormalities in wolves can cause serious mor-
bidity or mortality and include fractured teeth, pulpa necrosis,
severe periodontal disease, periapical bone loss, and mandibular
and maxillary fractures (Van Valkenburgh 1988, 2009). Wolves
with a dental root abscess, osteomyelitis due to pulpa disease,
tooth fractures, or severe periodontal disease may die as a result
of secondary septicemia, or simply from starvation, because of
pain and the inability to chew (Barber-Meyer 2012). Those that
survive are less able to compete when feeding on larger prey
and may lose weight, condition, and status (Miles and Grigson
1990; Barber-Meyer 2012). However, even lesions that are not
severe have an influence on morbidity (Pavlica et al. 2012).
For example, mild periodontal disease can lead to substantially
reduced longevity, and secondary lesions involving cardiac
valves, kidneys, and liver (Pavlica et al. 2012). Therefore, it is
important to report the occurrence of these less severe lesions.
About a dozen articles have been published concerning
oral lesions in wolves (Supporting Information S1). Some
reports are anecdotal case studies or document this condition
for few individuals (Theberge et al. 1994; Lazar et al. 2009;

1111
1112 JOURNAL OF MAMMALOGY
Barber-Meyer 2012), while others report larger numbers, rang-
ing from dozens in Croatia (n = 32—Pavlovic et al. 2007) and
in central Europe (n = 51—Stockhaus 1965) to more than
a 100 in Latvia (n = 187—Andersone and Ozolins 2000),
the Soviet Union (n = 324—Dolgov et al. 1964), the United
States (n = 112 and 373—Van Valkenburgh 1988, 2009),
the Soviet Union and Europe (n = 500—Vila et al. 1993),
Scandinavia (n = 131—Räikkönen et al. 2013), and Canada
(n = 241—Wobeser 1992). Because most studies focus only on
1 or a few types of oral lesions in larger groups (Buchalczyk
et al. 1981), it is not always clear if other lesions are absent
or just not reported. Most studies of larger samples focus only
on 1 or 2 easily observable abnormalities, such as the number
of teeth and severe tooth fractures, and make no mention of
concomitant oral abnormalities. This makes the information
gained incomplete, conclusions on morbidity incorrect, and
does not allow for comparisons between geographical or tem-
poral data sets.
A comprehensive protocol for a more complete and system-
atic assessment of oral lesions in wolf skulls is, however, lack-
ing. With such a framework, oral lesions across wolf subspecies
and populations could be mapped and compared, allowing
inferences about health status and ecology in the wild. The goal
of our study is to record the nature and prevalence of congeni-
tal and acquired dental abnormalities in skulls of Middle East
wolves using a standardized and thorough protocol, as is rou-
tinely used in veterinary oral exams of domesticated dogs. We
postulate that by applying this protocol, robust comparisons of
dental lesions in wolf skulls across geographic and taxonomic
groups will be possible.
Materials and Methods
We used a standardized and detailed protocol for oral exams
(Table 1), as applied in clinical practice of companion animals
(specifically dogs) and examined a group of 40 Middle East
wild wolves from 2 collections (Appendix I). All specimens
examined were wild wolves. We examined 33 Israeli wolf skulls
from the George S. Wise Faculty of Life Sciences, Department
of Zoology at Tel Aviv University, Israel (ZMTAU), and 7
skulls from The Natural History Museum in London, Great
Britain (BMNH). The skulls examined belonged to either
C. l. pallipes or C. l. arabs (Pocock 1935, 1939; Mendelssohn
1982; Hefner and Geffen 1999; Nowak 2003; Sharma et al.
2004; Cunningham and Wronski 2010; Mivart and Keulemans
2012; Bray et al. 2014). The sample of wolf skulls from the
ZMTAU collection was obtained by taking out 3 boxes (each
box containing all bones from 1 specimen) per drawer (every
drawer contained 5–9 boxes) without a priori verification of
oral lesions. The drawers had not been organized in any way
(location of find, age, weight, sex, date found). In this way, a
quasi-random sample of the collection was examined. Of the
33 ZMTAU skulls, 32 were C. l. pallipes and 1 was C. l. arabs.
The BMNH collection of wolves contained few specimens and
many were severely damaged due to bullet holes or trauma.
This left 7 intact skulls all marked as C. l. arabs. Two of these
were definitely not C. l. arabs as they had been shot at the Iran–
India border, a location where arabs does not occur (Hefner
and Geffen 1999; Nowak 2003; Cunningham and Wronski
2010), and were reidentified as C. l. pallipes.
Visible lesions were recorded during examination of the
skulls (Table 2) and by examination of digital photographs
made from rostral, buccal, and lingual views. Detailed images
were taken of specific teeth or regions with lesions. Information
recorded was based on predetermined and reproducible criteria
by means of an established classification adapted for use on dry
skulls (Verstraete et al. 1996; Abbot and Verstraete 2005). We
used a dog chart for oral/dental examination to record lesions
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(Emily and Penman 1994:7, figure 1.8) because the dental for-
mula of wolves is identical to that of dogs (Huxley 1880; Miles
and Grigson 1990). Our nomenclature for anatomy and lesions
follows that of the American College of Veterinary Dentistry
(AVDC—Harvey and Emily 1993; Emily and Penman 1994;
Lobprise and Wiggs 2000; AVDC 2015). Lesions identified
were periodontal disease (gingival inflammation, infection,
and gingival attachment loss), tooth fractures, pulpa disease
(infection and necrosis of the neurovascular bundle in the pulpa
cavity), abnormal number of teeth, abrasion (wearing of den-
tal areas by grinding), atypical attrition (wear of tooth tips),
enamel lesions, and malocclusions.
Periodontal disease classes (Fig. 1) are divided into 4 stages
of severity (Miles and Grigson 1990:525, figure 24.2). For stage
1, lesions are not visible on skulls, only on oral soft tissues and
the alveolar margin is parallel to the cementoenamel junction
(Fig. 1a). In stage 2, a small part of the root is visible (< 25%;
Fig. 1b). In stage 3, between 25% and 50% of the root length is
visible (Fig. 1c). In stage 4, most of the root is visible (Fig. 1d).
A special form of periodontal disease, called furcation lesion,
has the alveolar bone of 2 adjacent roots of 1 tooth retracted so
that a furcation lesion is visible under the crown. This lesion
coincides with stages 3 and 4 periodontal disease (Fig. 1e).
For tooth fractures (Fig. 2), we observed 4 different forms in
our skulls. These are enamel fractures, complicated and uncom-
plicated crown fractures, and infraction. We did not study other
types of tooth fractures such as root fractures (observable
only with radiographs) and crown-root fractures (e.g., Emily
and Penman 1994; Lobprise and Wiggs 2000; AVDC 2015).
Enamel fractures show areas with detached enamel chips and
intact underlying dentine (Fig. 2a). Postmortem enamel chips
can be distinguished from those created during life by observing
the fracture borders, which are crisp in postmortem specimens.
In uncomplicated fractures, enamel and dentine are fractured,
but the pulpa cavity is not exposed (Fig. 2b). In complicated
fractures, enamel, dentine, and the pulpa cavity are harmed,
leading to visible tooth discoloration and pulpa infection and
necrosis, plus eventual further spreading of infection through
the root canal tip into adjacent alveolar bone leading to focal
bone loss and a local abscess (Fig. 2c; see pulpa disease below).
Preparation and conservation fractures can be recognized by
the presence of preserved fractured fragments and clean, sharp
fracture edges without secondary changes in pulpa. A special
form of tooth fracture is infraction in which a series of parallel
 Table 1.—Terminology of oral/tooth lesions in wolf skulls.

1 Periodontal disease: inflammation of the attachment apparatus of the tooth in alveolar bone, often accompanied by infection
1.a Stage 1: gingivitis only; this pathology by definition cannot be observed on prepared skulls
1.b Stage 2: gingivitis plus gingival attachment loss, with alveolar bone loss less than 25%
1.c Stage 3: more than 25% but less than 50% loss of alveolar bone around root
1.d Stage 4: more than 50% loss of alveolar bone, widening of periodontal space, and tooth unstable in alveolus
 1.e Furcation: sometimes seen in stage 4 as a furcation lesion (“sort of tunnel”) from lateral to medial and observed between rostral and caudal roots of one tooth, between the crown and bone, visible or
palpable
2 Tooth fractures
2.a Enamel fracture: chip fracture or crack of enamel
   Fissure: tooth broken with a fissure line, fragments present and in place
 2.b Uncomplicated crown (or crown-root) fracture: fracture of enamel/dentine (or cementum) without pulp exposure. Visible by loss of a part of the tooth. Can be horizontal, vertical, oblique, chip fracture, or
comminuted
2.c Complicated crown (or crown-root) fracture: fracture of enamel/dentine (or cementum) with pulp exposure (acute)/pulpitis/pulp necrosis (subacute and chronic)
2.d Infraction: enamel cracks/fractures, visible as horizontal lines (often on canines)
3 Pulpa disease: pulpitis/inflammation/infection of the tooth pulpa due to 1) trauma with tooth fracture into the root canal or tooth/root displacement with rupture of the root tip blood and/or nerve supply or
2) severe periodontal disease
3.a Discoloration seen as darkening of the tooth with intact enamel
3.b Pulpa necrosis seen as open/empty pulpa cavity (due to facture or excessive wear)
3.c Periapical bone loss with local cyst/granuloma/abscess/focal osteomyelitis at the root tip
3.d Local osteomyelitis of the mandibular of maxillar bone surrounding the tooth root
4 Abnormal number of teeth
4.a Missing teeth
   4.a.a Hypodontia (genetic): no alveolus present
   4.a.b Traumatic: tooth is missing, alveolus visible and deformed
4.b Excessive teeth: polyodontia/hyperodontia (genetic)
5 Abrasion
 5.a Abrasion: loss of tooth structure (starting with enamel loss) due to external factors such as gnawing/biting on stones, hard bones, fences, or tin cans or due to abrasive sand in food, mostly seen on vertical
tooth plane, dentine visible
5.b Cage biter syndrome abrasion: a specific form of abrasion, the wear is specifically seen on the caudal side of the canines due to biting and pulling on metal bars
 5.c Sand eating abrasion on incisors due to eating food on sandy surface or flea biting on the lower back
6 Attrition: loss of tooth structure due to wear of opposing teeth (6.a), starting at the crown, mostly seen on horizontal planes of teeth (6.b), a physiological age-related process depending on abrasiveness of type
of food. Dentine is exposed and when advanced also the pulpa canal, which will fill with black dentine (6.c; a physiologic phenomenon)
JANSSENS ET AL.—ASSESSING ORAL LESIONS IN WOLF SKULLS

7 Enamel hypoplasia/defect: due to severe general disease at young age (most frequently viral canine distemper) or local trauma to a deciduous tooth causing infectious pulpits: the underlying mature teeth will
then show enamel defects
7.a Mild enamel hypoplasia: brownish enamel discoloration
7.b Severe enamel hypoplasia: part of tooth is enamel free, dentine visible
8 Malocclusion
8.a Mesiocclusion: mandibular incisors more rostral than normal (overbite)
8.b Distocclusion: mandibular incisors more caudal than normal (underbite)
8.c Level bite: incisal edges or tips in occlusal contact with each other
8.d Post-traumatic malocclusion: after malunion of mandibular or maxillary fractures or tooth fractures/dislocation with displacement
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 Table 2.—Details of oral pathology per individual skull and classified per pathology type (see Table 1) in this series of Canis lupus arabs/pallipes. The numbers that follow categories
(e.g., periodontal disease) and the categories themselves are the same as explained in Table 1. Accession numbers in bold represent Canis lupus arabs. 1114

ID wolf Periodontal Tooth Pulpa Number Abrasion Attrition Enamel Malocclusion Total
disease (1) fracture (2) disease (3) of teeth (4) (5) (6) dysplasia (8)
(7)
1.b 1.c 1.d 1.e 2.a 2.b 2.c 2.d 3.a 3.b 3.c 3.d 4a.a 4a.b 4.b 5.a 5.b 6 7.a 7.b 8.a 8.b 8.c 8.d
ZMTAU 09439 15 1 1 1 1 18
ZMTAU 09460 11 11
ZMTAU 10334 11 1 12
ZMTAU 10338 0
ZMTAU 10355 1 1 2
ZMTAU 10402 1 1 1 1 1 2 10 1 18
ZMTAU 10608 16 1 1 1 1 20
ZMTAU 10609 0
ZMTAU 10610 0
ZMTAU 10615 6 1 1 2 1 1 2 1 15
ZMTAU 10619 16 1 2 19
ZMTAU 10621 9 1 10
ZMTAU 10682 14 1 2 1 18
ZMTAU 10685 6 1 1 1 1 1 11
ZMTAU 10686 5 2 2 2 1 1 13
ZMTAU 10688 11 1 12
ZMTAU 10692 10 1 11
ZMTAU 11041 18 18
ZMTAU 11109 20 1 4 25
ZMTAU 11110 8 5 1 2 4 1 21
ZMTAU 11118 1 1 1 3 7 13
ZMTAU 11119 13 1 1 1 16
ZMTAU 11121 1 23 24
ZMTAU 11250 1 1 2
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ZMTAU 11275 2 1 2 5
ZMTAU 11417 12 1 1 13
ZMTAU 11418 18 1 1 20
ZMTAU 11475 7 4 3 2 16
ZMTAU 11476 22 1 1 24
ZMTAU 11479 13 1 1 1 16
ZMTAU 11516 38 1 1 1 1 42
ZMTAU 11685 16 16
ZMTAU 12130 16 16
BMNH ZD.1891.2.5.1 8 2 2 1 2 5 20
BMNH ZD.1895.10.8.1 12 3 1 1 2 1 1 1 12 34
BMNH ZD.1897.1.14.4 7 14 1 1 1 12 4 1 41
BMNH ZD.1899.11.6.36 4 1 5
BMNH ZD.1924.8.13.1 1 1
BMNH ZD.1940.193 8 2 1 1 10 22
BMNH ZD.1948.368 18 18
Total teeth 372 53 10 7 1 3 13 12 7 5 2 8 8 9 3 32 8 23 2 39 2 1 2 1 591
Grand total teeth 442 29 22 20 40 23 41 6 591
Total skulls 27 9 7 5 1 3 10 7 6 5 2 6 8 9 3 4 3
Grand total skulls 33 15 11 17 6 3 7 6

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 JANSSENS ET AL.—ASSESSING ORAL LESIONS IN WOLF SKULLS 1115

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Fig. 1.—Periodontal disease: a) A normal molar tooth (without periodontal disease) in a prepared skull (right mandibular M1), labial view, roots
are well covered by bone. The alveolar margin runs parallel to the enamel; b) Stage 2 periodontal disease. Labial view. Both roots of the left man-
dibular P4 have periodontal disease. The arrows point at the caudal root and mark the retracted alveolar mandibular bone ventrally and dorsally the
original height of attachment of healthy oral mucosa. The root is partially denuded due to loss of alveolar bone (less than 25% of total root length);
c) Stage 3 periodontal disease. Labial view of the rostral root of the left maxillar P4. The root is partially free of alveolar bone (between 25% and
50% of the total root length); d) Stage 4 periodontal disease. Labial view of the rostrolateral root of the left maxillar M2. This root is visible for
most part due to loss of alveolar bone (more than 50% of the total root length); e) Furcation lesion. The arrow points at the furcation lesion seen
between rostral and caudal roots of the left mandibular M2. Labial view.

Fig. 2.—Tooth fractures: a) Enamel fracture. Only the enamel layer is fractured or fissured. Here visible in the right mandibular C. Lingual–caudal
view; b) Uncomplicated fracture of the right maxillar M2. Labial view. Enamel and dentine are fractured, dentine is visible but the pulpa canal is
unharmed; c) Complicated crown fracture. The enamel, dentine, and pulpa canal are part of the fracture. Here visible is M1 of the left mandible.
A transverse fracture of the cranial part of the tooth is visible with concurrent bony lesions caused by secondary local infection with bone loss.
Labial view; d) Infraction. A series of parallel enamel cracks which are horizontal in appearance. Here visible on the caudal side or the left maxil-
lar canine. Labial view.

enamel cracks, horizontal in appearance, are present in canine lesions. First, there is discoloration (Fig. 3a) with pulpa and
teeth (Fig. 2d). dentine (not enamel) being discolored, usually dark red or
Pulpa disease (Fig. 3) is most often related to tooth trauma, brown. Second is pulpa necrosis. At first, the pulpa is exposed
although severe periodontal disease can also cause these after trauma, followed by infection, then necrosis (Fig. 3b). On
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Fig. 3.—Pulpa disease: a) Discoloration, seen as darkening of the tooth with intact enamel. Here visible on maxillar I1 and I2 on the right side (see
arrows). Rostral view; b) Pulpa necrosis due to trauma and seen as open pulpa cavity in C1 left maxilla. Ventral/oblique view; c) Periapical bone
loss with local cyst/granuloma/abscess/focal osteomyelitis at the root tip. Left maxillar C1, labial view; d) Local osteomyelitis. Abscess at the top
of the caudal root of the left maxillar P4 with a draining tract opening (arrow). The maxillar bone surrounding the opening is spongy, caused by
local infection and periostal reaction. Labial view.

skulls, the infection presents itself as an open canal colored
black or dark brown. Root tip abscesses (Fig. 3c) are a further
(third) temporal step in the pathophysiology of infected pulpa,
when bacteria invade the alveolar bone adjacent to the root tip
to form a local abscess. In the last (4th) and most severe class
of pulpa disease, root tip infection spreads to the adjacent bone
causing osteomyelitis and a cortical bone-perforating draining
tract (Fig. 3d).
The next lesion is an abnormal number of teeth (Fig. 4).
Hyperodontia can occur (Fig. 4b) or teeth can be absent
(hypodontia; Fig. 4a). Hyperodontia is genetic in origin, whereas
hypodontia occurs when teeth in prepared skulls are absent due to
preparation (no lesions), trauma, or genetic causes. Preparation
absence is easy to determine as a clean, deep, sharp-edged alveo-
lus of an entire tooth is discernable. Traumatically lost teeth can
sometimes be partially lost, in which case fractured remnants of
roots are still visible in the alveolus. If the tooth is totally lost
due to trauma, the alveoli in which roots were located will grad-
ually fill with alveolar bone, leaving a scar-like, small elevation
or pocket at the original location of the root (Fig. 4a.2). Thus, it
is possible to discern trauma-related tooth loss from hereditary
hypodontia. In the latter case, the mandibular or maxillary bony
ridge is flat and straight (Fig. 4a.1).
Abrasion (Fig. 5) is the erosion of a part of the tooth through
abnormal mechanical external processes. It is most frequently
related to gnawing or biting on hard structures, such as stones or
bones (Fig. 5a) or grinding substances like sand (Fig. 5b). Cage
biter syndrome (Fig. 5c) is a specific form of abrasion only on
the caudal surface of canines. It is generally associated with
biting on metal (such as fences and bars) and is not reported
in dogs that bite and gnaw on bones, as enamel is harder than
bone. Abrasion of the rostral aspect of incisors gives an indi-
cation of intensive coat nibbling (usually associated with flea
infestation) or feeding on erosive sandy surfaces and can pro-
vide information about eating habits and/or external parasites.
Attrition (Fig. 6) is the physical erosion of crown tips by
friction induced by biting and gnawing. In our series of skulls,
physical, age-related attrition (Van Valkenburgh 1988; Anders
et al. 2011) was not recorded. It was only recorded when asym-
metric or allocated to only a few teeth. A special form of attri-
tion is seen in level bites where upper and lower incisor tips
are in contact (Fig. 6a). In attrition, teeth tips wear at a very
slow rate. First enamel wears down and the underlying dentine
becomes visible (Fig. 6b). As this process continues, the hollow
pulpa canal will start to fill with dark-colored dentine, which
then shows as a dark “bull’s eye” in surrounding dentine with
an enamel border (Fig. 6c). In canine teeth, this will lead to
typical concentric dark circles, with the outer concentric ring
being enamel (ivory color). Near the center, the polished ivory-
colored dentine is present, and centrally, the dark (black to very
 JANSSENS ET AL.—ASSESSING ORAL LESIONS IN WOLF SKULLS
Fig. 4.—Abnormal number of teeth: a.1) Hypodontia. Absent P1 in the right maxilla. Intraoral dorsal view; a.2) Traumatic tooth loss. The arrow
points at a lost I1 in the right maxilla. The alveolus is filled with bone. Rostral view; b) Hyperodontia. Excessive teeth. The left mandible shows
an extra M4. Labial view.
dark brown)-colored reactively filled (with dentine) pulpa canal
can be observed (Fig. 6d).
Mild enamel hypoplasia is recognized by enamel discolor-
ation and/or surface irregularities with enamel thinning, seen as
irregular, undulated areas of enamel (Fig. 7a). Severe enamel
hypoplasia consists of areas absent of enamel, with dentine
being exposed (Fig. 7b). This can be seen as pits, planes, or
ripples. A specific form of enamel lesions consists of a horizon-
tal enamel hypoplasia line spread over several adjacent teeth
(Fig. 7c—Miles and Grigson 1990:448, figure 20.16), which
is typically caused by a Morbillivirus infection (canine distem-
per) during growth and tooth eruption (Fiani and Arzi 2009).
Malocclusion (Fig. 8) consists of mesiocclusion (under-
bite), distocclusion (overbite), level bite, and post-traumatic
malocclusion seen after fractures with malunion (bony union
with deformed anatomy). In normal bite, the upper incisors are
positioned rostral from the lower incisors and are in close con-
tact. In mesiocclusion, the maxillary incisors are positioned
caudally from the mandibular incisors (Fig. 8a). In distocclu-
sion, the mandibular incisors are positioned much too caudally
relative to the maxillary incisors (Fig. 8b). In level bite, tips
of incisors from the mandible and maxilla touch each other
(Fig. 8c).
To minimize the likelihood of major differences in the num-
ber of lesions between the 2 subspecies, we tested for differ-
ences in each of the lesion classes between wolf subspecies
(arabs, n = 6 and pallipes, n = 34). A generalized linear model
(GLM) was used with a log link function and a Poisson error
distribution test for differences in the number of lesions in
each of the classes between wolf subspecies (arabs, n = 6 and
pallipes, n = 34), a GLM was used with a log link function
and a Poisson error distribution. An extra dispersion parameter
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was estimated to account for overdispersion. In this model,
the number of lesions was the dependent variable, and sub-
species the explanatory variable, i.e., a factor. This analysis
is an analysis of variance (ANOVA)-type test because the
number of lesions is compared between groups. However, an
ANOVA with associated F-test would be inappropriate in this
case because the data are not normally distributed. Counts, as
in this case the number of lesions, are typically Poisson dis-
tributed. A GLM with a Poisson error distribution and using a
log link function is thus appropriate. The linear model can be
written as:
log(number of lesions) = µ 0 + α + ε
where µ0 represents the natural logarithm of the mean num-
ber of lesions for pallipes, α the difference in mean number of
lesions with arabs (on a logarithmic scale), and ε the error term.
The significance test of the null hypothesis that α = 0, i.e., no
difference, was based on an F-distribution, taking into account
the overdispersion (due to many 0s in the data set). Because 24
comparisons were performed, we used a Bonferonni correction.
Results
Results of the GLM were not significant. Comparisons between
the 2 subspecies were not statistically significant at the 5% level
for any of the lesions classes. We therefore decided to present
the results below combined across the 2 subspecies.
A total of 40 skulls representing 1,680 teeth were exam-
ined. Lesions observed are presented in Table 2 and in the
Supporting Information S1. Teeth missing due to preparation
were not counted as lesions. A total of 591 lesions were found
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Fig. 5.—Abrasion: a) Extreme abrasion with intact pulpa in the right-sided maxillar C1; b) Incisor abrasion of the maxillar I. Due to flea biting or
eating sand contaminated food; c) Cage biter syndrome in maxillar canines. The caudal enamel of the canines is eroded; d) Cage biter syndrome
on the caudal side of mandibular canines.

among the 1,680 teeth (35%), and the total percentage of skulls
with lesions was 92.5% (37 skulls). Periodontal disease was
encountered in 33 skulls (82.5%) and 442 teeth (26%). Stage 2
was especially prevalent (372 teeth or 19%).
Noncomplicated tooth or enamel fractures were observed
in 4 skulls (10%) and 4 teeth. Complicated tooth fractures
with exposed pulpa were observed in 10 skulls (27.5%) and
13 teeth. Fractures mostly involved incisors and canines (5 and
14, respectively). Infraction was seen in 12 teeth in 7 skulls
(17.5%). In total, 29 tooth fractures were seen in 15 different
skulls (37.5%).
Pulpa disease was found in 11 skulls (27.5%) and 22 teeth.
Discoloration was encountered in 7 teeth in 6 skulls, pulpa
necrosis in 5 teeth and skulls, and root abscesses, periapical
bone loss, draining tract, and local osteomyelitis in 10 teeth
and 8 skulls.
Abnormalities in the number of teeth were present in 17
skulls (42.5%). Hypodontia was seen in 8 (20%); mostly
premolars were missing. Missing teeth due to traumatic dislo-
cation and loss were seen in 9 skulls (22.5%). Three skulls had
hyperodontia with 1 supernumerary tooth (7.5%); in 1 skull a
premolar and in 2 skulls a mandibular 4th molar.
Abrasion was observed in 5 skulls (12.5%) and 40 teeth.
Evidence for cage biter syndrome was present in 3 skulls
(7.5%) and 8 teeth, but only at the level of the canines. Sand
abrasion in incisors was seen in 2 skulls and 20 teeth. Abnormal
attrition was documented in 6 skulls (15%) on different types
of teeth. In 1 skull, it was single sided and caused by avoid-
ance of biting on the side where a complicated crown fracture
with pulpa necrosis was present. Another had a 1-sided, cau-
dal mandibular, molar attrition. In the last skull, the problem
was symmetrical and located in 3 caudal mandibular molars.
Enamel hypoplasia was observed in 7 skulls (17.5%) and 41
teeth. In 2 of these skulls, an incremental horizontal hypoplasia
line was present affecting a total of 35 teeth (12 in 1 skull, 23
in the other).
 JANSSENS ET AL.—ASSESSING ORAL LESIONS IN WOLF SKULLS 1119

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Fig. 6.—Attrition: a) Attrition due to level bite as seen in incisors. Rostral view; b) Attrition. Here physiological age-related tooth wear or attrition
is present in all premolars and molars of the right maxilla (labial view); c) Attrition. Dentine is exposed and when more advanced also the pulpa
canal (arrows), which fill with black dentine (a physiologic phenomenon). Intraoral view of the left maxillar P4, m1 and 2; d) Typical attrition of
a canine tooth. Three concentric circles can be seen: the outer enamel circle, the central discolored, and darker pulpa cavity with reactively filled
colored dentine—a nonpathological process—and in between dentine.

Fig. 7.—Enamel lesions: a) Mild enamel hypoplasia at the labial side of the right maxillar C1. Apart from coloration changes (which is also seen
in pulpa discoloration), the color change is localized in the enamel itself and combined with enamel surface irregularities; b.1) Severe enamel
hypoplasia on the left mandibular apex of C1. Labial view; b.2) Severe horizontal line hypoplasia as seen after canine distemper infection dur-
ing growth. The enamel hypoplasia is located in between the 2 parallel lines and visible in C, P2, P3, and P4 of the right mandible. Labial view.

The frequency of malocclusion was 15% (6 skulls). Two Discussion

skulls showed mesiocclusion, 1 showed distocclusion, 2 had
The results of this study are unique in that no other studies have
level bite, and 1 a post-traumatic unilateral bite abnormality
either reported particular lesions reported by us or they have ab
with peripheral displacement (subluxation) of a canine and sec-
initio focused on specific lesions and thus may have overlooked
ondary penetration of the hard palate.
1120 JOURNAL OF MAMMALOGY
Fig. 8.—Malocclusion: a) Mesiocclusion. The maxillar incisors are positioned caudally from the mandibular incisors (underbite); b) Distocclusion.
The mandibular incisors are positioned too caudally in regard to the mandibular incisors (overbite); c) Level bite. Incisors from the mandible and
maxilla top on each other causing excessive attrition. Rostral view.
lesions that are included in our analysis (for an overview of oral
lesions reported by other authors, see Supporting Information
S1). Reported low rates of occurrence for some lesions may
thus represent an underestimate due to overlooked subtle vari-
ants. A standardized reference as presented here provides
a useful tool to allow a more systematic and comprehensive
assessment of lesion types across studies. Specific examples
are provided below.
Oral lesions reported elsewhere but not observed in our study
include permanent deciduous teeth, caries, locked foreign bod-
ies, microdontia, and deformed and rotated teeth (Dolgov et al.
1964; Van Valkenburgh 1988; Wobeser 1992; Vila et al. 1993;
Andersone and Ozolins 2000; Pavlovic et al. 2007; Barber-
Meyer 2012; Räikkönen et al. 2013). The nature of these lesions
and the fact that they are clearly visible when present indicate
they would be easily detected using our protocol. Thus, it seems
probable they were absent in specimens examined here.
Some studies have reported only 1 or a few easily diagnos-
able lesions. These studies were generally cranial morphomet-
ric studies that also looked at the number of teeth. Andersone
and Ozolins (2000) reported some broken teeth and Stockhaus
(1965) reported mesiocclusion and distocclusion. Van
Valkenburgh (1988, 2009) and Leonard et al. (2007) reported
only tooth fractures related to attrition in extant and extinct
Pleistocene carnivores. Also, Vila et al. (1993) focused on tooth
loss and its possible influence on survival. Unreported lesions
could, however, be identified using figures within these papers.
Van Valkenburgh (1988:292, figure 1) shows a stage 3 periodon-
tal disease in all roots of P1–3 and the rostral root of P4 in the
maxilla of a hyena, which was not reported as the study focused
only on fractures. Wobeser (1992), Theberge et al. (1994), and
Barber-Meyer (2012) report on a locked foreign body that over
time induced ever more severe lesions, starting with local infec-
tion (gingivitis and periodontal disease), and progressing to
gingival necrosis, exposure of maxillary palatal bone and tooth
roots, followed by local osteomyelitis, draining tract formation
and enamel necrosis, possibly with enamel chipping and tooth
fracture. Because these lesions all represent secondary events
that result from the initial problem of a locked foreign body, we
considered them to belong to a single category.
Other studies have focused on a wider variety of lesions,
but figures within those papers suggest that particular lesions
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were overlooked or not reported. Pavlovic et al. (2007) reported
on periodontal disease, local osteomyelitis, caries, and com-
plicated root fractures. Based on their figures, we identified
additional periodontal disease stage 2 in 8 roots and 5 teeth.
Their reported osteomyelitis can be further diagnosed as being
complicated by a visible pulpa necrosis. In another tooth, in
addition to their reported severe periodontal disease stage 4, a
fracture of the root can be observed, causing secondary osteo-
myelitis. Their reported caries should be diagnosed as attrition
because of a typically black coloration of the filled, reactive
pulpa canal. Caries is related to sugar-rich food, unavailable in
the wild. With the exception of Pavlovic et al. (2007), caries has
not been reported in wolves or feral dogs. Losey et al. (2014)
reported tooth fractures, tooth loss, trauma, and enamel hypo-
plasia and focused mainly on injuries to dogs that were likely
inflicted by humans. Thus, although their study entails a large
sample size (400 skulls), it does not report periodontal disease,
pathological abrasion, or attrition and pulpa disease. Lazar
et al. (2009) reported missing teeth, malocclusion, complicated
and noncomplicated tooth fractures, pulpa disease, abrasion
on the rostral side of canines, root tip abscess, and periodontal
disease stage 4 with focal osteomyelitis and draining tract, all
observed in a single specimen. Following the criteria applied in
our study, the reported fractured maxillary canines show traits
that rather link it to the condition of severe attrition, not frac-
ture (Lazar et al. 2009:87, figure 3). Räikkönen et al. (2013)
reported a population of inbred wolves and documented many
oral abnormalities. One image of a skull (p. 4, figure 2) shows
periodontal disease stage 2 in the caudal root of mandibular P3,
and severe enamel hypoplasia, and appears very much like cage
biter syndrome, but is not reported. Miles and Grigson (1990)
report a variety of lesions, including periodontal disease, a
locked foreign body, malocclusion, hyperodontia, and 1 case
of enamel hypoplasia. Enamel hypoplasia was also reported by
Losey et al. (2014) in 2.5% of skulls, which is considerably less
than in our study (17.5%). It is possible that many authors do
not recognize enamel hypoplasia or have considered it to be a
preparation error.
Periodontal disease was reported in some studies: Miles
and Grigson (1990) reported it in 2% of animals, Pavlovic
et al. (2007) in 10% of skulls, and Lazar (2009) in a single
skull. These values are much smaller than those reported in the
 JANSSENS ET AL.—ASSESSING ORAL LESIONS IN WOLF SKULLS
present study. It may be that periodontal disease occurs more
frequently in Middle East wolves due to different feeding hab-
its or genetic susceptibility. Several of the studies noted above
did not report the presence of periodontal disease, giving an
overall frequency of occurrence of these lesions (in > 3,000
skulls total for all studies) that is astonishingly low compared to
our study (we reported a prevalence in 26% of the teeth and in
82.5% of the skulls). It is likely that only the most severe stages
were reported in these studies. We report stages 3 and 4 in only
6% of skulls, which is similar to the percentage reported for the
other studies.
It has been reported that Middle East wolves forage on
human garbage and thus consume relatively soft food (Hefner
and Geffen 1999). Consumption of soft food makes wolves,
just as dogs, susceptible to development of periodontal lesions
(Talbot 1899; Hamp and Lindberg 1977; Vosburg et al. 1982;
Miles and Grigson 1990). Moreover, African wild dogs (Lycaon
pictus) that feed only on wild prey exhibit periodontal lesions
in 41% of cases (Steenkamp and Gerhard 1999) which is con-
siderably lower than in our study. On the other hand, in our
series of skulls, those from the preindustrial period (and pre-
sumably not feeding on human garbage) do not show less peri-
odontal disease than those that lived recently (Table 2). Genetic
susceptibility is one possible explanation for this. Periodontal
disease has a genetic component (Peyer 1973; Watson 1994).
Dogs have a very high incidence of periodontal disease and a
recent study suggests that the Middle East wolf was the pro-
genitor of dogs (Vonholdt et al. 2010). However, more recent
genetic research suggests a Eurasian origin with the Middle
East wolves being a closely related subspecies (Thalmann et al.
2013). If this subspecies is genetically close to dogs, it could
explain the high incidence of periodontal disease (Vonholdt
et al. 2010). However, we postulate that the most important
explanation for the difference of occurrence is simply under-
reporting in previous studies.
Overall, it is clear that the type and extent of oral lesions in
wild wolf populations has not been reported consistently or
accurately. Our analysis of 40 skulls using proposed diagnostic
traits to distinguish between the different pathological catego-
ries is an effort to remedy this situation. This approach identi-
fies clearly diagnosable lesions and thus provides data on the
frequency of lesion types in a population. The ability to identify
and assess the prevalence of different lesion types is crucial, not
only to permit comparisons across populations and studies but
also for using these observations as reliable proxies for behav-
ior and overall health conditions within these populations. For
example, while cage biter syndrome is linked to domesticated
dogs, it can reflect chewing on fences or feeding on human gar-
bage (e.g., tin cans) in wild wolves (Hefner and Geffen 1999;
Cunningham and Wronski 2010; Tourani et al. 2013). Two addi-
tional examples exemplify the link between dental lesions and
health of wolf populations: the correct identification of linear
enamel hypoplasia may indicate the prevalence of Morbillivirus
in a population (Fiani and Arzi 2009), and minor stages of peri-
odontal disease suggest reduced longevity and a higher preva-
lence of lesions involving chronic low-grade infections of the
1121
cardiac valves and kidneys caused by repetitive release of oral
bacteria into the bloodstream. More severe periodontal lesions
may be indicative of possible secondary septicemia, oral pain,
reduced ability to gnaw or bite, and subsequent loss of weight
and condition (Miles and Grigson 1990; Pavlica et al. 2012).
There was no statistical difference in lesions between the 2
wolf subspecies. It is important to note this may be due to the
difference in group size, and especially the small number of
C. l. arabs (n = 6). The latter resulted in a relative small statisti-
cal power hindering detection of subtle differences.
The framework proposed here will make possible the correct
identification of oral lesion types and degrees of severity and
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can serve as a guideline for both researchers and wildlife man-
agers working with wild wolves. Use of this framework will
provide a standardized format and facilitate future comparative
studies across geographic and taxonomic groups. It can pos-
sibly also be used in other carnivore species, and its criteria
can probably be generally applied across taxa with long-lived
animals.
Acknowledgments
We are grateful to R. Fleisher and K. Helgen from the
Smithsonian Institute for guidance. C. Smeenk and S. van der
Mije from the National Museum of National History in Leiden,
The Netherlands, are thanked for helping in the search for suit-
able skulls; P. Jenkins and R. Portela Miguez from the Natural
History Museum London are thanked for allowing us to exam-
ine the available collection of Canis lupus arabs and pallipes
skulls; C. Lefevre, A. Abourachid, and H. Lellèvre from the
Paris Museum of Natural History are thanked for searching
their collection; M. Nussbaumer and P. Schmid from the Bern
Museum of Natural History are thanked for helping with the
search for appropriate skulls and their examination; F. Voltera
is thanked for informing on specimen available in Belgian
museums; and S. Meiri from the Tel Aviv Faculty of Life
Sciences is thanked for helping and allowing us to visit and
examine their collection. Very special thanks go to F. Verstraete
for scientific help and advice. S. van Dongen is thanked for
statistical advice and A. Gautier for his critical reading. S. De
Cauwer is thanked for helping with the careful preparation of
the table layout. D. Jaggar is thanked for all the time and energy
he put in linguistic assistance. Also “thank you” to all authors
that answered our mails requesting for extra information. This
article was written based on sympathy for the endangered car-
nivore: the Middle Eastern wolf. http://videos.howstuffworks.
com/animal-planet/6636-global-wolf-endangered-middle-east-
ern-wolves-video.htm. Accessed 20 February 2016.
Supporting Information
The Supporting Information documents are linked to this
manuscript and are available at Journal of Mammalogy online
(jmammal.oxfordjournals.org). The materials consist of data
provided by the author that are published to benefit the reader.
The posted materials are not copyedited. The contents of all
1122 JOURNAL OF MAMMALOGY
supporting data are the sole responsibility of the authors.
Questions or messages regarding errors should be addressed
to the author.
Supporting Information S1.—Oral lesions as reported in ref-
erenced articles and this article with their occurrence reported in
approximate percentages (%) and the number (N°) of wolf skulls.
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 1124
Appendix I
List of the wolf skull samples. The Israeli collection from George S. Wise Faculty of Life Sciences, Department of Zoology at Tel Aviv University (ZMTAU) and the
London, British Museum of Natural History collection (BMNH) represent 33 and 7 skulls each. Collection identity numbers, genus, species, subspecies, and sex are pre-
sented as are country, region, and locality where the specimen was caught, found, or shot. Accession numbers in bold represent Canis lupus arabs.
Accession number Genus Species Subspecies Sex Collection date Country Region Locality
ZMTAU 09439 Canis lupus pallipes M 1905 Israel Gallilei ?
ZMTAU 09460 Canis lupus arabs F 1905 Saudi Arabia Sandiya Abha
ZMTAU 10334 Canis lupus pallipes F 2005 Israel Galilei Shamir
ZMTAU 10338 Canis lupus pallipes F 2003 Israel Galilei Lahavot Habashan
ZMTAU 10355 Canis lupus pallipes F 2005 Israel Golan Merom Golan
ZMTAU 10402 Canis lupus pallipes F 2003 Israel Golan Yahudiyya
ZMTAU 10608 Canis lupus pallipes M 2003 Israel Galilei Shamir
ZMTAU 10609 Canis lupus pallipes M 2003 Israel Golan Mahane Romah
ZMTAU 10610 Canis lupus pallipes F 2004 Israel Golan ?
ZMTAU 10615 Canis lupus pallipes F 2004 Israel Golan Nahal Maitsar
ZMTAU 10619 Canis lupus pallipes F 1905 Israel Golan Golan
ZMTAU 10621 Canis lupus pallipes F 2004 Israel Golan ?
ZMTAU 10682 Canis lupus pallipes M 1905 Israel Golan Gamla
ZMTAU 10685 Canis lupus pallipes M 2003 Israel Golan Nahal Kanaf
ZMTAU 10686 Canis lupus pallipes F 1905 Israel Golan Tel Hispin
ZMTAU 10688 Canis lupus pallipes M 2002 Israel Golan Golan
ZMTAU 10692 Canis lupus pallipes M 2002 Israel Golan ?
ZMTAU 11041 Canis lupus pallipes F 1905 Israel Galilei Lahavot Habashan
ZMTAU 11109 Canis lupus pallipes M 1905 Israel Galilei Shamir
ZMTAU 11110 Canis lupus pallipes M 2004 Israel Golan Fajer Nahal Suach
ZMTAU 11118 Canis lupus pallipes M 2004 Israel Galilei Shamir
ZMTAU 11119 Canis lupus pallipes F 2004 Israel Golan Ortal, North Golan
ZMTAU 11121 Canis lupus pallipes F 2004 Israel Golan Ortal, North Golan
JOURNAL OF MAMMALOGY

ZMTAU 11250 Canis lupus pallipes M 2005 Israel Galilei Kefar Szold
ZMTAU 11275 Canis lupus pallipes M 2005 Israel Galilei Kefar Szold
ZMTAU 11417 Canis lupus pallipes M 2005 Israel Galilei Shamir
ZMTAU 11418 Canis lupus pallipes F 2005 Israel Golan Maagar Yosiphon
ZMTAU 11475 Canis lupus pallipes M 2005 Israel Negev Ruhama
ZMTAU 11476 Canis lupus pallipes M 2005 Israel Golan Nov
ZMTAU 11479 Canis lupus pallipes M 2005 Israel Galilei Lahavot Habashan
ZMTAU 11516 Canis lupus pallipes M 2006 Israel Golan Ramat haGolan
ZMTAU 11685 Canis lupus pallipes M 2006 Israel Golan Kanaf
ZMTAU 12130 Canis lupus pallipes M 2007 Israel Gallilei Moledet
BMNH ZD.1897.1.14.4 Canis lupus arabs F 1897 Saudi Arabia Jaquakar Burkab
BMNH ZD.1891.2.5.1 Canis lupus arabs ? 1891 Saudi Arabia Bouraida Qasin
BMNH ZD.1895.10.8.1 Canis lupus arabs M 1895 Yemen Aden ?
BMNH ZD.1899.11.6.36 Canis lupus arabs M 1899 Oman Muscat ?
BMNH ZD.1924.8.13.1 Canis lupus pallipes ? 1924 Iran ? ?
BMNH ZD.1940.193 Canis lupus arabs F 1940 Saudi Arabia Jeddah Jeddah
BMNH ZD.1948.368 Canis lupus pallipes ? 1948 India ? ?

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