Naturwissenschaften (2013) 100:235–243
DOI 10.1007/s00114-013-1018-5
ORIGINAL PAPER
A Pathological Late Pleistocene canid from San Sidero
(Italy): implications for social- and feeding-behaviour
Dawid Adam Iurino & Rosario Fico & Mauro Petrucci &
Raffaele Sardella
Received: 20 October 2012 / Revised: 11 January 2013 / Accepted: 14 January 2013 / Published online: 1 February 2013
# Springer-Verlag Berlin Heidelberg 2013
Abstract Evidence of diseases on vertebrate fossil bones
can provide detailed information on many aspects of extinct
animals. This study focused on pathological craniodental
remains (left maxilla and dentary) referred to the canid
Cuon alpinus unearthed from a Late Pleistocene karst filling
deposit at San Sidero (Apulia, southern Italy). These fossils
show clear evidence of a chronic periodontitis that caused
the animal’s death. Clinical diagnosis of the disease and the
timing of its development have been defined on the basis of
a veterinary odontostomatology approach, in addition to
radiographic and tomographic techniques. From the initia-
tion of the infection until death, a time span of at least
6 months occurred, and three main steps have been defined:
(1) the bacterial infections of the buccal cavity turning into
severe periodontitis, (2) the fracture of the lower carnassial
and (3) the loss of teeth due to the worsening infection that
deformed and/or eroded maxillary and mandibular bones
and enlarged alveoli. The analysis of the palaeopathology
also provides information about the biomechanics of the
bite, on the feeding behaviour and on the relationships of
injured members in a pack of Late Pleistocene canids.
Communicated by: Robert J. Asher
D. A. Iurino : R. Sardella
Dipartimento si Scienze della Terra, Sapienza Università di Roma,
Piazzale Aldo Moro 5,
00185, Rome, Italy
D. A. Iurino (*) : M. Petrucci : R. Sardella
IsIPU, Istituto Italiano di Paleontologia Umana, via Aldrovandi 18,
00197, Rome, Italy
e-mail: dawid.iurino@uniroma1.it
R. Fico
Istituto Zooprofilattico Sperimentale del Lazio e della Toscana,
via Appia Nuova 1411,
00178, Rome, Italy
Keywords Palaeopathology . Tomography . Carnivora .
Cuon alpinus . Late Pleistocene . Italy
Introduction
Palaeopathology in vertebrate palaeontology focuses essen-
tially on the skeletal system because bones and teeth are
much better preserved than other anatomical tissues
(Moodie 1917; Benton 2005; Waldron 2009). The most
common observed pathologies are fractures and dental
anomalies (Moodie 1917; Rossi et al. 2004; Aufterheide
and Rodrìguez-Martìn 2006; Rothschild and Martin 2006;
Waldron 2009), with variability depending (for example) on
taxon and individual age. Discoveries of pathology in ver-
tebrate fossil bones are relatively frequent (Moodie 1917),
but they are poorly investigated despite their importance in
reconstructing the ontogeny, physiology and palaeoecology
of fossil taxa.
Among vertebrate pathologies, periodontitis is of particular
interest because of its considerable effect on teeth and max-
illary/mandibular bones and, as a consequence, on mastication
and feeding behaviour. Periodontitis is an infection of bacte-
rial origin that may cause loss of teeth, tissue inflammation,
abscess formation, deformation and remodelling of mandibu-
lar, premaxillary and maxillary bone tissues (Neville et al.
2002; Ortner 2003; Aufterheide and Rodrìguez-Martìn 2006;
Radostits et al. 2006; Waldron 2009). In the most serious cases
of chronic disease, the animal cannot survive (Aufterheide and
Rodrìguez-Martìn 2006).
The goal of this work is to describe periodontitis in
remains of Cuon alpinus from the Late Pleistocene of San
Sidero (Apulia, Italy) using tomographic techniques and
veterinary diagnostics (Ashraf 2011; Chhem and Brothwell
2008; Sutton 2008).
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Extant C. alpinus, Lycaon pictus and Canis lupus are
characterized by complex social structures, a condition
probably shared also with closely related Pleistocene forms.
Behavioural ecology provides data about this topic which
can be used in the interpretation of some palaeoecological
aspects of the fossil species. In this case, the pathologies of
the San Sidero dhole (Cuon alpinus) provide also evidence
for sociality in this Pleistocene species.
Materials and methods
Radiography and CT
Radiographs have been taken at the Veterinary Clinic “La
Clinica Veterinaria Borghesiana” (Roma), using digital
Radiological Unit Rx Foschi x1 425 HF. It consists of an X-
ray tube of KW 16–32, with rotating anode of 2,800 rpm (HZ
50) and 60 mm in diameter. The maximum anode voltage is
130kV. Radiographs have been made in projection L-L (lat-
ero-lateralis) 42 kV; mAs 20, projection M-L (medio-lateralis)
42 kV; mAs 20, with dimensions of 3,072×3,072 pixels.
Tomographic images have been made at M. G. Vannini
Hospital by Philips Brilliance CT 64-channel scanner. The
fossil of C. alpinus was scanned in its entirety in the coronal
(i.e. transverse of some authors) slice plane from front to
back. The scanning resulted in 210 slices (i.e. images) for
the maxilla and 183 for the dentary, with dimensions of
768×768 pixels. The slices are 0.45 mm thick with an
interslice space (the space between consecutive slices) of
0.20 mm. Segmentation and 3D rendering of the maxilla and
dentary were computed using the Open-Source software
Osirix 3.9.4, 32-bit for Mac.
Systematic palaeontology
Mammalia Linnaeus, 1758
Carnivora Bowdich, 1821
Canidae Fischer de Waldheim, 1817
Cuon Hodgson, 1838
Cuon alpinus Pallas, 1811
Type locality
“Udskoi Ostrog,” reported in Honacki et al. (1982) as
“U.S.S.R., Amurskaya Obl., Udskii-Ostrog.”
Etymology
Generic name Cuon derives from the Greek κύων (=dog),
latinized Cuon Hodgson, 1838. Specific epithet alpinus
should mean “alpine, from Alps,” but Pallas (1811) did
not provide a clear explication of this term.
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Referred material
SS 2004/1: left maxilla with I3, C, P2–P4, M1
SS 2004/2: left dentary with P1–P3, fragment of P4, frag-
ment of M1, M2
“SS” refers to San Sidero. Specimens are housed in the
Earth Science Department of Sapienza University of Rome.
Geological setting
In 2004, during a field survey at San Sidero locality
(Maglie, Lecce, Apulia, 40°08′20″ N, 18°16′23″E)
(Fig. 1), a research team of the Earth Sciences Department
of Sapienza University of Rome unearthed a maxillary bone
and associated dentary of a large individual of the canid C.
alpinus.
San Sidero is located in a region where several quarries
are opened for the extraction of a Miocene calcarenite,
known as “Pietra Leccese.” During the Middle–Late
Pleistocene, the calcarenite was affected by intense karst
activity that formed an articulated fissure network that the
quarry activities have since exposed (Selleri et al. 2003;
Selleri 2007). The vertically funnel-shaped karst fissures,
locally named “ventarole,” were filled with “terre rosse,” i.e.
residual reddish clays rich with iron oxides, including, in
some cases, vertebrate fossil bones. The fossil remains,
carried by surface water run-off in the fissures, are generally
well preserved, and articulated bones can be found. The
faunal assemblage recorded into the “terre rosse” deposit
includes Equus ferus, Equus hydruntinus, Stephanorhinus
hemitoechus, Dama dama, Cervus elaphus, Capreolus cap-
reolus, Bos primigenius, Bison priscus, Sus scrofa, Canis
lupus, Canis mosbachensis, C. alpinus, Vulpes vulpes,
Panthera pardus, Felis silvestris, Lynx lynx, Crocuta cro-
cuta, Meles meles, Lepus europaeus, Oryctolagus cuniculus,
Erinaceus cf. E. europaeus, Microtus (Terricola) savii, and
Fig. 1 Location of the Late Pleistocene site of San Sidero (Maglie,
Apulia, southern Italy)
Naturwissenschaften (2013) 100:235–243
Apodemus sylvaticus, Eliomys quercinus and has been bio-
chronologically referred to the beginning of the Late
Pleistocene (De Giuli 1983; Bologna et al. 1994; Bedetti et
al. 2004).
Cuon alpinus
Cuon alpinus (Pallas 1811), or dhole, is a medium-size
social canid, with brown or reddish coat, usually character-
ized by a conspicuous white spot that extends from the
throat to the abdomen (depending upon the geographical
region), and a dark bushy tail (Fig. 2a, b). In extant Cuon,
body weight is about 15–17 kg for males and 10–13 kg for
females (Fox 1971, 1984; Venkataraman and Johnsingh
Fig. 2 Cuon alpinus (Pallas 1811) from San Sidero (Maglie, Apulia,
southern Italy); Late Pleistocene. a Life reconstruction of the animal; b
reconstructed head; c complete skull; d San Sidero fossils of C.
alpinus; e1–g2 maxilla and dentary of San Sidero dhole (scale bar
237
2004). The current distribution of the genus Cuon includes
some areas of Southeast Asia (India, Malaysia, Sumatra and
Java), but the historical range included China, Mongolia and
Eastern Russia. During the Late Pleistocene, the distribution
reached Eurasia and North America (Baryshnikov 1996;
Ripoll et al. 2010; Brugal and Boudadi-Maligne 2011).
In Italy, the dhole has been recorded from the late Middle
Pleistocene to the earliest Holocene, and it is documented by
teeth, jaws and incomplete post-cranial remains (Del
Campana 1923; Fabiani 1923; Boule and De Villeneuve
1927; Del Campana 1954; Bedetti et al. 2004; Petrucci et
al. 2012).
The dhole occupies different habitats, preferring dense
forest and thick scrub jungle, avoiding deserts (Nowak
30 mm); e1 illustration buccal view; e2 illustration lingual view; f1
photo buccal view; f2 photo lingual view; g1 radiography buccal view;
g2 radiography lingual view. al apical lesion, pd periodontal disease.
Photo and illustrations by D. A. Iurino
238
2005). The teeth show that Cuon is a typical hypercarnivo-
rus canid, like Lycaon and Speothos, adaptively converging
on the latter (Thenius 1954a, b; Ewer 1973; Macdonald and
Sillero-Zubiri 2010). They are hunters, socially organized in
packs of five to ten individuals, rarely 30 (Davidar 1973,
1975; Fox 1984). The prey tends to be medium to large
mammals like deer, wild pigs, mountain sheep, gaurs and
antelopes. They are tracked by scent and then pursued,
sometimes for a considerable distance. Overtaken, it is sur-
rounded and attacked from different sides. When flesh
availability is scarce, dholes may also hunt alone or in pairs,
taking smaller prey (Davidar 1973, 1975; Fox 1984;
Venkataraman et al. 1995).
Description
The C. alpinus described here includes an articulated left
premaxilla and maxilla (SS 2004/1) and a left dentary (SS
2004/2). The bones belong to the same individual, and both
of them show pathologies (Petrucci et al. 2012). The mate-
rial is stored in the Earth Science Department of Sapienza
University of Rome (Fig. 2e1–f2).
The premaxilla and maxilla bear the third incisor, the
canine, the second, third and fourth premolars, and the first
Fig. 3 Cuon alpinus (Pallas 1811) from San Sidero (Maglie, Apulia,
southern Italy); Late Pleistocene. a, b C. alpinus dentary (scale bar
30 mm); c, d C. alpinus maxilla (scale bar 30 mm); a photo occlusal
view; b 3D CT image occlusal view; c photo occlusal view; d 3D CT
image occlusal view; e fractured P4, photo on the left and 3D CT
images on the right (scale bars 5 mm); f 3D CT images of
Naturwissenschaften (2013) 100:235–243
molar. The I3 and the canine are lightly worn on the apex
and along the mesial and distal sides. P1 is absent, and the
alveolus is completely closed by newly formed porous bone
tissue. P2 and P3 are complete and unworn. The cusps of the
upper carnassial do not show wear, but the anterior root is
broken, posterior to which is a very slender root. M1 has the
talon basin crown traumatically removed after chewing of a
hard object. At level of P4 and M1 a trauma/infection pa-
thology (periodontitis) involves the teeth and the surround-
ing bone tissue, and both show traces of calculus (a kind of
hardened dental plaque) (Fig. 3c, d, k).
The dentary lacks of incisors, canine and the coronoid
process. P1, P2, P3 and M2 are complete and unworn,
whereas P4 and M1 are fractured. The trauma involves
the dentary, too, clearly fractured at the level of P4 and
M1. The horizontal branch is deformed, and the fourth
premolar lacks the posterior half of the crown and related
root, while in the lower carnassial the posterior root and a
little portion of the crown are present. The attribution to
the species C. alpinus (Petrucci et al. 2012) is strengthened
by the X-ray image analysis that shows the absence of the
M3 alveolus behind the M2 (Fig. 2g1, g2) (Ewer 1973). At
present, both fossils constitute the most complete cranio-
dental sample of Cuon in Italy.
hemimandibular teeth (scale bar 10 mm); g fractured M1, photo on
the left and 3D CT image on the right (scale bars 5 mm); h odontopathic
fistula (scale bar 5 mm); i worn canine (scale bar 5 mm); j post-
mortem fracture on the left and additional root on the right (scale
bars 10 mm), RE root exposure; k tartar on M1 (scale bar 5 mm).
Photo by D. A. Iurino
Naturwissenschaften (2013) 100:235–243 239

Diagnosis

Periodontitis is defined as “Inflammatory disease of teeth

supportive tissue, caused by specific microorganisms which
lead to progressive destruction of periodontal membrane
and alveolar bone, with formation of periodontal pockets
and gingival recession” (Pejčić et al. 2007).
Dogs show a natural predisposition to be affected by
acute peridontitis, as a consequence of pre-existing gingivi-
tis (Strillou et al. 2010). Periodontitis could be caused and
worsened by the diet of soft foods, promoting the accumu-
lation of supragingival plaque and calculus.
This acute pathology may evolve in chronic periodon-
titis due to the response to bacterial aggregations on the
tooth surfaces. The outcome is an irreversible destruction
of the connective tissue attachment, which results in
periodontal pocket formation and loss of alveolar bone
(Brown et al. 1989).
For the Apulian fossils SS 2004/1 and SS 2004/2, the
hypothesis of a chronic periodontitis can be supported by
an increase of the alveolar bone tissue pores through
which the blood flows. Shape, diameter and “architecture”
of blood vessels are strongly influenced by a chronic
pathologic condition.
In canids, a chronic inflammation of the oral cavity Fig. 4 CT scanning visualization of teeth details of San Sidero fossil.
a1 P4 with evident enlargement of pulp cavity due to chronic inflam-
provokes an increasing of the gingival blood flow (from mation (in red) (scale bar 10 mm); a2 coronal section of P4 with
200 to 400 %) (Kaplan et al. 1982). Moreover, the persistent additional root (in red) (scale bar 5 mm); b coronal section of M1, in
tissuesinflammation provokes an increasing development of evidence the pulp cavity (in red) (scale bar 10 mm); c lingual view of
the vascular pores in the maxillary and dentary bones M2, in evidence the gingival pocket (scale bar 5 mm). ar additional
root, epc enlargement of pulp cavity, gp gingival pocket, pc pulp
(Kaplan et al. 1982; Hock and Kim 1987; Zoellner 1990), cavity, pd periodontal disease
as can be observed in the fossil Apulian Cuon SS 2004/1
and SS 2004/2.
The prevalence and severity of gingivitis and periodonti- from the roots of the teeth, a symptom of chronic periodon-
tis in dogs increase principally with age, but the nature of titis caused by a bacterial infection protracted for a long time
infection, genetics and diet can vary the affection between (Aufterheide and Rodrìguez-Martìn 2006; Waldron 2009).
individuals/individually (Strillou et al. 2010). Veterinary The destructive osteomyelitis process has also caused a
studies on colony dogs point out that periodontitis appears significant thickening of the maxillary bone of the section
earlier and more severely than in domestic dogs (Page and between P4 and M1. The porosity involves the whole bone
Schroeder 1981). tissue that surrounds the periodontal area, indicates a rich
Signs of osteomyelitis were evident on SS 2004/1 and SS blood supply due to chronic inflammation (Söderholm and
2004/2. A protracted bacterial infection caused the patholo- Egelberg 1973). An odontopathic fistula is present on the
gy, forming gingival pockets (Fig. 4c) and odontopathic palate near P4, probably connecting an abscess or apical
fistulas, and provoking partial or total loss of teeth and granuloma to oral cavity (Fig. 3h). Calculus is evident on
retraction of newly formed bone tissue. the P4 paracone and metastyle external surfaces and is more
The anterior side of upper canine and posterior side of I3 abundant on the M1 paracone and metacone labial side
crown are strongly worn due to malocclusion (Fig. 3i). The (Fig. 3k).
analysis of the radiographic image of the jaw shows that the By the radiographic and CT scanning images, radiopaque
loss of the P1 has led to the resorption of the alveolus with borders around the root apices of P4, M1 and P4 are clearly
the formation of spongy bone tissue. This is a clue that the visible. These empty cavities are named apical lesions and
animal survived several months after the loss of the tooth are produced by bacterial activity. In some cases, inflamma-
(even traumatic, because of the lack of signs of periodonti- tion continues along the dental roots (Carranza et al. 2011)
tis) (Fig. 3c, d). Along the labial surface, from the posterior as evident in the P4 (Fig. 4a1). A tiny and non-functional
edge of P3 to M1, there is a clear detachment of the bone root is present on the labial side of the upper carnassial,
240
evident on X-ray and CT images (Figs. 3j and 4a2). Such a
condition is not very common, but it has been recorded in
some carnivores (Verstraete et al. 1996). The fracture of the
anterior root of P4 occurred post-mortem, during fossiliza-
tion. In the dentary, alveoli of P4 and M1 are partially
occluded by spongy bone, related to a cyst or apical granu-
loma. On the distal side of the M1, a gingival pocket is
visible (Fig. 4c). The thickening of horizontal branch is
caused by destructive/regenerative processes of the perios-
teum or bone remodelling due to inflammatory stimulus.
The fractures involving P4, P4 and M1 were made during
life since they are complementary in the occlusion points
and simultaneously involved in the biomechanics of the bite
(Fig. 3e, g). The traumatic event took place during this
phase. The fracture did not cause the immediate loss of
teeth, allowing the onset of bacterial infection during the
subsequent months. Great variability in the course of a
periodontal disease can be observed in modern canids, and
on the basis of the large diameter of the cavities left by the
blood vessels evident between P4 and M1 and exposure to
most of the P4 and M1 roots, the disease of the San Sidero
dhole started more than 6 months before the animal’s death.
Such a time has been estimated following the experimental
models provided by Nyman et al. (1978) and Strillou et al.
(2010). These authors pointed out that the seriousness of the
alveolar bone loss can be classified by measuring the dis-
tance between the upper edge of alveolar bone and the
cementum-enamel junction (Fig. 3j).
Measurements carried out on spontaneous or experimen-
tal cases showed that 4–6 months are needed to provoke a
root exposure of 5 mm (Strillou et al. 2010; Kinoshita et al.
1997; Pallua and Suschek 2011). In SS 2004/2, the alveolar
bone loss ranges between 3 and 15 mm; thus, the inferred
development time of the periodontitis can be defined as
more than 6 months.
Discussion
Developmental pathology
The pathology of the San Sidero dhole caused malocclusion
and compromised the capacity of the animal to bite. Such a
condition led to a heavy wear of left I3 and upper and lower
canines that were involved in shearing and chewing. As
observed in extant canids affected by the same disease, the
chewing was probably compensated by the lower and upper
right tooth rows (Pavlović et al. 2007; Lazar et al. 2008).
The effects can be observed mainly on the anterior teeth
of left dentary and maxilla, where the posterior side of I3 and
the anterior side of the upper canine have been heavily worn
by anomalous movement of the lower canine. This caused
enamel and partially dentine wear (Aufterheide and
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Rodrìguez-Martìn 2006) (Fig. 3i). The cause of the dental
fractures is unclear although the morphology of the frac-
tured surface seems to indicate a strong compression
(Neville et al. 2002). This would be confirmed by the
breaking lines of the P4 and M1 crown, which follows the
points of minimum thickness. Probably, the trauma did not
occur during predation, when incisors and canines are main-
ly used (Ewer 1973; Tumlison et al. 1989; Valkenburgh
1996, 2009) but perhaps during feeding activity and/or
chewing a hard object. Since there is no evidence of frac-
tures or tooth marks on the fossils, we exclude the possibil-
ity that the initial traumatic event was due to predation or
fighting injuries caused by other animals.
The trauma did not cause directly the damage to P4 and
M1. These teeth broke when the bone tissue underlying the
teeth was retracted, and the tooth pulp that caused strong
and chronic pain to the animal was exposed (Figs. 3e, g and
4b). As a consequence, the absence of the occlusion caused
the lowering of P4. The dramatic increase of pathology may
have led to the animal’s death, perhaps indirectly through
other associated diseases, as can be observed on extant
carnivores in similar conditions (Verstraete et al. 1996;
Lazar et al. 2008).
Excepting the heavily worn I3 and upper canine, the teeth
show slight wear, indicating an adult but not an old individ-
ual. The pattern of tooth wear in the extant dhole (Durbin et
al. 2004) suggests an age between 2 and 4 years for the
animal from San Sidero; this inference is supported by the
analogy with the estimating age by tooth wear in other
canids (Ferrara 1965; Gipson et al. 2000). Other diagnostic
features are unavailable, such as cranial suture closures.
Similar considerations can be used also for reconstructing
the final weeks of the Late Pleistocene dhole from San
Sidero. Although Cuon could prey on small animals and
insects, and eat plants sporadically (Macdonald and Sillero-
Zubiri 2010), this kind of diet cannot allow the survival of
an isolated sick individual for many months. The severe
pathology affecting the animal left heavy evidence of the
disease development following three phases until death,
lasting more than 6 months (Nyman et al. 1978; Strillou et
al. 2010): (1) development of bacterial infections of the
buccal cavity of the dhole, followed by periodontitis; (2)
the fractured carnassials possibly by biting a very hard
object and ( 3) loss of the teeth due to the worsening caused
by the infection that deformed and/or eroded maxillary bone
and mandibular bones and enlarged alveoli.
Feeding behaviour inference
Efficiency in providing food is of crucial importance for a
carnivore, and surviving a disease for months depends on
different factors (Valkenburgh 1996, 2009). Many large
canids, such as dholes, African wild dogs and wolves, are
Naturwissenschaften (2013) 100:235–243
social species, and such a condition has been taken into
account to explain the possible pack support for an animal
in a severe state of disease. Behavioural ecology provides
information which can be used in the interpretation of some
palaeoecological aspects of fossil species.
An interesting case study was presented by Palmqvist et
al. (1999). These authors described the skull and the man-
dible of a large hypercarnivorous canid from the Early
Pleistocene site of Venta Micena (Spain). The fossil, later
referred to Lycaon lycaonoides (Martínez-Navarro and
Rook 2003), shows dental anomalies; it lacks the right I1,
I2, C1,P2, the right M2 and M3, and the right I3 and P1 are
partially fractured. Palmqvist et al. (1999) explained the
survival of the animal with such an abnormal craniodental
condition through cooperative behaviour. In fact, some
authors report that the cooperation of many wild dogs within
a pack could support injured individuals (Kruuk and Turner
1967; Palmqvist et al. 1999).
A detailed analysis of the feeding behaviour, in particular,
regarding hypercarnivorous canids, was required in order to
better define a complex and well-structured hierarchical soci-
ality (Thenius 1954a, b; Ewer 1973; Fox 1984; Venkataraman
et al. 1995; Macdonald and Sillero-Zubiri 2010; Srivastav and
Nigam 2010).
In these species, especially in wolves and dholes, the
food is hierarchically shared, and the dominant male/female
is the first to feed (Fox 1984; Srivastav and Nigam 2010).
Among African wild dogs and uniquely, among canids,
puppies first have access to the prey, followed by all the
other members of the pack (Malcolm and Marten 1982). In
all these cases, no special attention is given to sick animals
within the pack.
According to this model, we can assume that the
Pleistocene dhole from San Sidero, was still able to chew
and to be part of the pack, at least during the first phase of
the disease. Thus, the animal was probably one of the last to
have access to food, being a young adult individual (2–
4 years old). Due to the deterioration of its health caused
by osteomyelitis, the animal was no longer able to partici-
pate effectively in hunting activity. Therefore, the assistance
through food regurgitation to a sick animal with limited
predatory and locomotory abilities by other members of
the pack seems to be the most likely hypothesis to consider.
It has been suggested in the case of the Venta Micena
Lycaon (Palmqvist et al. 1999; Martínez-Navarro and
Rook 2003).
Although cases in which wild dogs have regurgitated
food to other adults are known in literature (Kruuk and
Turner 1967; Estes and Goddard 1967), these episodes are
considered exceptions and not as a manifestation of habitual
behaviour. Among wolves, African wild dogs and dholes,
regurgitation is a practice mainly targeted towards puppies
and lactating females and in some cases, towards individuals
241
that guard juveniles (Malcolm and Marten 1982; Fox 1984;
Courchamp and Macdonald 2001; Courchamp et al. 2002).
On the contrary, healthy or sick adult individuals do not
typically receive any direct assistance in food sharing
(Fentress and Ryon 1982; Fox 1984); although among wild
dogs, food sharing may be more flexible, and some cases of
regurgitated food to injured or sick members of the pack
have been reported (Kruuk and Turner 1967; Estes and
Goddard 1967). Etho-ecological studies pointed out that
such behaviour within the pack is closely related to its
energy cost (Malcolm and Marten 1982; Courchamp and
Macdonald 2001; Courchamp et al. 2002). For example,
pack size in canids has a great influence in the amount of
regurgitation that individuals can receive. Within the pack,
there is a clear relationship between the number of hunting
individuals, the prey size and the amount of food carried to
the den to be shared with cubs and females. In times of food
scarcity, the sentinels at the den are not fed. On the other
hand, a greater number of hunters can bring a larger amount
of food to the den, with a consequently increase of the
availability of food per capita (Malcolm and Marten 1982;
Creel and Creel 1995; Gusset and Macdonald 2010;
Courchamp and Macdonald 2001; Courchamp et al. 2002).
According to this, the hypothesis of direct help to injured
members of the pack cannot be supported. A possible and
more realistic explanation suggests considering the whole
pack as a strong “protective condition” for individuals with
reduced capabilities. Therefore, a sick individual can sur-
vive within the pack as a sort of “intraspecific kleptopar-
asite,” being indirectly supported by the other components
of the pack and receiving protection. It could be described as
passive support of the pack, which provides protection
against other predators, such as large felids and hyaenas,
and provides prey killed by the other members of the pack
(Courchamp and Macdonald 2001).
The severe pathology of the dhole from San Sidero has
been investigated in detail thanks to CT scanning and image
processing techniques, which provide information also on
the effect that periodontitis and other associated diseases
produced on teeth and bone tissues.
We estimate that the animal could have survived since
onset of the infection for 6 months. This is in accordance
with a social condition that protects the sick animal against
other predators and provides food sources. Finally, on the
basis of the behavioural ecology studies on the extant social
canids quoted above, the occurrence of an “indirect” support
of the pack, with no evidence of a “direct altruistic behav-
iour,” can be suggested.
Acknowledgments We would like to thank Dr. Paolo Peppucci and
Dr. Aniello Polise (La Clinica Veterinaria Borghesiana, Rome, Italy)
for their help in making the first radiographic investigations. Dr.
Massimiliano Danti and Prof. Sabino Della Sala (Ospedale M.G.
Vannini, Rome, Italy) for making the CT scanning. Dr. Claudia Eleni
242
and Dr. Cristiano Cocumelli (Istituto Zooprofilattico Sperimentale del
Lazio e della Toscana, Italy) for their advice in the first phase of this
work. Prof. Luigi Boitani, Prof. Alessandro Pilolli, Dr. Luca Santini
(Sapienza University of Rome), Dr. Martina Jeżowska (Karolinska
Institutet, Sweden) and Dr. Fiore Conca for their useful suggestions
and help. The authors also express their gratitude to Dr. Sven Thatje,
Dr. Robert Asher and two anonymous reviewers who greatly improved
this article with constructive criticisms, comments and suggestions.
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