Introduction
The lion is part of the Felidae family, and one of the four large cats of the Panthera
species, along with the tiger, panther, and wild leopard. Europe, Asia, the Middle
East, and large parts of Africa were once the main regions of habitat for the lion
(Panthera leo ).[1 ]
[2 ] Now, they are mostly found in savannah and grasslands throughout sub-Saharan Africa,
while many are kept in zoos throughout the world.[3 ] Over the years, there were reports of abnormalities in the skulls of the lions at
these zoo-gardens of Europe,[4 ] South Africa,[5 ] Australia,[6 ] the United States,[7 ] and Asia.[8 ] The skull forms the head skeleton, which protects the brain and organs of special
sense, such as the eyes, ears and nose, besides housing teeth for mastication. The
head is important in body coordination and defense as well as olfaction and deglutition.[9 ] The skull of an animal contributes to the phylogenetic structure of the head of
animal species, as seen in the feline or in the camel.[10 ] Further, the morphology of the skull gives rise to the animal's taxonomic affiliations,[11 ]
[12 ] and the occipital bone of the skull can be used in forensic medicine to determine
its gender.[13 ] The foramen magnum of the skull has scientific importance due to its clinical and
variant morphological importance,[14 ] and any deviation in its form and structure can lead to neurological indications.[15 ] There are no available literatures describing the osteology of the skull and mandible
of the lion. Thus, the main purpose of this article is to give a detailed description
of the gross anatomy of the bones and foramina of the lion's skull and mandible. This
description would be useful in the identification of the skull and mandible of the
lion, as well as to help the zoo veterinarians in the detection, diagnosis, and treatment
of head affections in this species.
Materials and Methods
The heads of two lions that died in the zoo in Trinidad and Tobago were brought to
the department of basic veterinary sciences, School of Veterinary Medicine, Faculty
of Medical Sciences, University of the West Indies, Trinidad and Tobago. No skeletal
deformities were detected upon inspection of the heads, which were then boiled and
treated to remove the skin and muscles, then bleached in 3% hydrogen peroxide and
then left to dry.[16 ] The different standard views of the skull and mandible were then photographed, followed
by radiographic photography taken for documentation using a Kodak digital camera and
Siemens mobile full wave X-ray machine (Siemens Medical Solutions, Erlangen, Germany),
respectively. The bones and foramina of the skull were named according to Nomina Anatomica
Veterinaria.[17 ]
Results
The Bones and Foramina of the Facial Region
The facial part of the skull of the lion was relatively large and compressed laterally.
The bony part of the dorsal, lateral and medial aspect of the face was made up of
the nasal, premaxilla, lacrimal, zygomatic, maxilla, palatine, pterygoid, vomer and
turbinate bones. In the ventral part of the skull, the hard palate was observed and
was made up of the palatine processes of the premaxilla and palatine bones. It appeared
as V-shaped at its caudal margin. In the ventral view, the choanae were seen at the
terminal part of the hard palate, and the cribriform plate served to separate the
nasal cavity from each of the cranium.
The nasal bones were paired, and flattened and triangular in shape in the nasal cavity.
They articulated with the frontal, maxillary and incisive bones, and their oral end
was comma shaped. The nasal bones were free from notches and foramina. A deep longitudinal
depression was seen in the dorsal aspect of the nasal bones. The caudal projection
of the nasal-frontal suture extended more caudal than that of the maxillary-frontal
suture. The lateral and ventral walls of the nasal cavity were formed by the premaxillae
or incisive bones, which were paired and rounded. Each of the premaxilla bones had
less developed nasal and palatine processes. In the rostral portion of each premaxilla,
the alveoli for the three upper incisors were observed along with a well-defined space
for the lower canine tooth frame ([Figs. 1 ]
[2 ]
[3 ]).
Fig. 1 Gross and radiographic images showing the rostral (A-D) and lateral (B-C) aspects
of the skull of the African lion. 1-Premaxilla bone; 2-Maxilla bone; 3-Zygomatic bone; 4-Frontal process of zygomatic
bone; 5-Nasal bone; 6-Frontal bone; 7-Zygomatic process of frontal bone; 8-Lacrimal
bone; 9-Temporal bone; 10-Zygomatic process of temporal bone; 11-Parietal bone; 12-Nuchal
crest; 13-Hamulus of pterygoid bone; 14-External sagittal crest; 15-Pterygoid bone;
a- Palatine fissures; b-Upper incisor; c-Upper canine; d-Infraorbital foramen; e-Internasal
suture; f- Nasofrontal suture; g-A longitudinal dorsal depression in the nasal and
frontal bones; h-Orifice of the nasolacrimal duct; i-Sphenopalatine foramen; j-Ethmoidal
foramen; k-Optic foramen; l- Foramen orbitorotundum; m-Alar foramen; n-Frontomaxillary
suture.
Fig. 2 Gross photos of the rostral aspect (E-F); Radiography of the caudorostral aspect (G)
and cranium of the skull of the African lion (H). 1-Premaxilla bone; 2-Maxilla bone; 4-Frontal process of zygomatic bone; 6-Frontal
bone; 7-Zygomatic process of frontal bone; 18-Occipital condyle; a- Palatine fissures;
b-Upper incisors; c-Upper canine; d-Infraorbital foramen; e-Internasal suture; f-Nasofrontal
suture; g-A longitudinal dorsal depression in the nasal and frontal bones; n-Frontomaxillary
suture; o-Nasomaxillary suture; p-A groove for lower canine tooth; k-Optic foramen;
l-Foramen orbitorotundum; m-Alar foramen; y-Oval foramen; B-Foramen magnum; C-Frontal
sinus; D-Cribriform plate; E-Hypophyseal fossa.
Fig. 3 Gross and radiographic images (I-L) showing the ventral aspect of the skull of the
African lion. 10-Zygomatic process of temporal bone; 12-Nuchal crest; 13-Hamulus of pterygoid bone;
16-Horizontal part of palatine bone; 17-Presphenoid bone; 18-Occipital condyle; 19-Jugular
process; 20-Mastoid process; 21-Tympanic bulla; 22-Retroglenoid process; 23-Mandibular
fossa; 24- Basioccipital bone; 25-Muscular process; 26-External occipital protuberance;
27-Vomer bone; (18); a-Palatine fissures; b-Upper incisor; c-Upper canine; r-upper
premolars; s-Upper molar; t-Major palatine foramen; v-Jugular foramen; w-Foramen lacerum;
x-Caudal alar foramen; y-Oval foramen; z-External acoustic meatus; A-Hypoglossal canal;
B-Foramen magnum.
The cranial rim of the orbit of the lion was bounded by the lacrimal bones, which
articulated with the zygomatic, maxillary and frontal bones. They presented the lacrimal
segment only, and they also presented the orifice of the nasolacrimal duct. The zygomatic
bones were well developed with a quadrilateral shape, and they had the frontal processes,
which, with the well-developed zygomatic processes of the frontal bones, tended to
close the orbital arches. They had the temporal processes, which contributed to form
the massive zygomatic arch with zygomatic processes of the temporal bones ([Fig. 1 ]).
The maxillae were the most developed and largest bones in the face. They were attached
to the premaxilla, nasal, lacrimal and frontal bones, and formed the wall of the hard
palate. The dental edges of the maxillary bones presented the dental alveoli for one
canine, three premolars, and one molar. The paired palatine bones were observed in
the palate and orbit and circumscribing the choanae. They had the perpendicular and
horizontal processes. The horizontal process and the palatine process of the maxilla
formed the oral palatine foramen. The pterygoid bones were delicate bones, which had
a very developed hamulus in their caudal aspect. They formed the roof and lateral
walls of the nasopharyngeal passage, while the vomer bone was an elongated, thin unpaired
bone, which contributed to the nasal cavity cranially and articulated with the premaxilla,
presphenoid and maxilla bones. In the nasal cavity, the turbinate bones were attached
to its lateral walls as delicate, scroll-like, complex bony plates. The foramina of
the facial region of the skull were the large infra-orbital foramen representing the
maxillo-incisive or infraorbital canal opening, the sphenopalatine foramen, the oral
palatine fissures, the orifice of the nasolacrimal duct and the choanae ([Figs. 1 ]
[2 ]
[3 ]).
The Bones and Foramina of the Cranial Region
The cranium was moderately compressed latero-medially and slightly flattened dorsoventrally
in the fronto-orbital region. The frontal, parietal, temporal, basioccipital, basisphenoid,
and presphenoid bones formed the bony part of the dorsal, lateral, ventral, and caudal
aspects the basicranial region in the lion. The frontal bone formed the roof of the
skull and contributed to the temporal fossae and orbital cavities. It had the short
zygomatic processes with neither supraorbital groove nor foramen, and it attached
to the nasal bones cranially. A deep longitudinal depression was seen in the frontal
region. The bulk of the roof of the skull was formed by the parietal bones, which
had a less prominent temporal line and a well-developed external sagittal crest. The
presphenoid bone was seen in the nasopharyngeal passage as a single bone and consisted
of a body and two orbital wings. The basisphenoid bone was a single bone between the
presphenoid bones and the basilar part of occipital bone and it consisted of a body,
two wings. The nuchal crest of the occipital bone was prominent, angular and directed
caudally. The median occipital crest was thick and more prominent in its proximal
part. The tympanic bulla was large, while the mastoid process and jugular processes
were small, and the muscular tubercle was not prominent. The basilar tubercles were
not observed. The temporal bones contributed to the glenoid cavity, the brain case
and the zygomatic arch by its zygomatic process. The intraparietal bone was not seen
externally, as it was merged with the parietal bone to form the highest caudal part
of the external sagittal crest. The temporomandibular joint of the lion was formed
between the coronoid process of the mandible and the glenoid fossa of the skull. The
foramina of the basicranial region were the external and internal acoustic meatuses
and foramen magnum, foramen lacerum, and hypoglossal canal in the condyloid fossa.
The foramina of the pterygopalatine fossa at the caudal aspect of the orbit on the
wing of the presphenoid includes the ethmoidal, optic, orbitorotundum, rostral alar,
and oval foramina, in addition to the caudal alar and jugular foramina. The ethmoidal
fossa was deep with extensive cribriform plate and the frontal sinus was observed
only in the frontal bone. Moreover, the hypophyseal fossa was prominent within the
cranium on the dorsal surface of the basisphenoid bone ([Figs. 1 ]
[2 ]
[3 ]
[4 ]).
The Mandible and Its Foramina
The mandible was the largest paired bone of the head region of the lion, in which
the right and left portions were fused rostrally at the mandibular symphysis. The
joint formed was fibrocartilaginous and not ossified. Each part of the mandible consisted
of a body and a ramus. The ramus had coronoid, condylar and angular processes along
with the masseteric and pterygoid fossae. The condylar process was directed ventrally,
and it articulated with the glenoid cavity of the skull at the temporomandibular joint.
The coronoid process was a well-developed large process directed slightly caudally,
forming the dorsal part of the ramus. The angular process directed caudo-medially.
The ramus of the mandible has the strongly excavated masseteric fossa with a well-developed
crest located on its lateral surface and the pterygoid fossa, which was smooth and
presented the mandibular foramen on the medial surface of the ramus. The dorsal border
of the mandible housed the dental alveoli for three lower incisors, one canine, two
premolars and one molar. The diastema was observed as the space between the lower
incisors and premolars. There were two mandibular foramina on the two rami of the
mandible on the pterygoid fossae, near the angular processes, while there were two
mental foramina on each side of the body of the mandible laterally ([Fig. 4 ]). The dental formula of the lion was 30 teeth; Incisor (I) 3/3, canines (C) 1/1,
premolars (Pm) 3/2, molar (M) 1/1 × 2= 30.
Fig. 4 Gross and radiographic images showing the caudal aspect of the skull (M) and the mandible
(N-Q) of the African lion. 10-Zygomatic process of temporal bone; 12-Nuchal crest; 14- External sagittal crest;
18-Occipital condyle; 19-Jugular process; 20-Mastoid process; 26-External occipital
crest; 28-Coronoid process; 29-Condylar process; 30-Angular process; 31-Masseteric
fossa; 32-Ramus of the mandible; 33-Body of the mandible; 34-External occipital protuberance;
B-Foramen magnum; G-Lower canine; F-Diastema; H-Lower incisors; I-Lower premolars;
J-Lower molar; K-Mandibular foramen; L-Mental foramina; M-mandibular symphysis.
Discussion
There was no available literature on the osteology of the skull and mandible of the
African lion, except the comparative splanchnocranium study between the brown bear
and lion.[1 ] The present results, as well as those in bears, lions,[1 ] tigers,[18 ] horses,[19 ] blackbucks,[20 ] and in dogs,[21 ] stated that the nasal bone was articulated cranially with the incisive bone, while
it also articulates with the lacrimal bone in camels[22 ] and in oxen.[23 ] Moreover, the caudal projection of the nasal-frontal suture extended more caudal
than that of the maxillary-frontal suture; a similar result was mentioned in tigers,[24 ] while the same author stated that the two caudal projections of the two sutures
were a line together in lions.
The premaxilla of the lion was very thick and had three dental alveoli for the upper
incisor teeth; a similar result was mentioned in bears, in lions,[1 ] and in tigers,[18 ] while it has no alveoli in blackbucks,[20 ] and in oxen.[23 ] Moreover, it had a well-defined space for the lower canine tooth frame in the lion.[1 ] The palatine process of the premaxilla shared in the formation of the bony hard
palate in the lion, as mentioned in blackbucks[20 ] and in oxen.[23 ] Furthermore, the palatine fissures were rounded in lion; a similar result was recorded
in the same animal, while they were oval in bears and in lions.[1 ]
The lacrimal bone of the lion presented the lacrimal segment only, and it also presented
the orifice of the nasolacrimal duct; a similar result is noticed in lions and brown
bears,[1 ]
[25 ] while the lacrimal bone is composed of a facial and a lacrimal part that fuse together
in horses,[19 ] in blackbucks,[26 ] and in oxen.[23 ] However, the lacrimal bone of sambar deer is marked by a very prominent depression
for infraorbital gland.[27 ]
The zygomatic bone of the lion was well developed, and its frontal processes did not
articulate with the zygomatic process of the frontal bone; a similar result was mentioned
in bears and lions.[1 ] The latter articulation is present in blackbucks,[26 ] and in oxen.[23 ] On the other hand, the zygomatic bone is absent in tigers.[18 ] Moreover, the zygomatic arch was very large with distinct ridges for masseter in
lion as mentioned in the same animal.[28 ] On the other hand, the zygomatic process of frontal is absent in rhinoceros.[29 ]
The maxilla of the lion was the most developed massive bone in the face, with neither
facial crest nor facial tuberosity; a similar result was mentioned in tigers,[18 ] in dogs[20 ] and in leopard cats.[26 ] However, the facial crest and tuberosity are present in blackbucks,[20 ] and in oxen,[23 ] while horses have the facial crest only.[19 ] Moreover, the maxilla of camel lacks the maxillary tuberosity and facial crest.[30 ] Furthermore, the maxilla had the dental alveoli for one canine, three premolars,
and one molar in the lion, while the maxilla has one canine, one vestigial tooth,
one premolar and one molar in lions, and one canine, one vestigial tooth, two premolars
and one molar in bears.[1 ]
The frontal bone formed the roof of the skull, and it had the zygomatic processes
and was characterized by the presence of a deep longitudinal depression, while the
external surface of the frontal bone is smooth in brown bears.[25 ] Moreover, the supraorbital foramen was absent in the lion; a similar result was
mentioned in tigers,[18 ]
[31 ] in dogs,[21 ] in adult sloth bears,[32 ] in arctic foxes,[33 ] and in common opossum.[34 ] The supraorbital foramen is present in blackbucks,[20 ] and in oxen.[23 ] There are two to three in number in Sambar deer.[27 ] The frontal sinus was observed only in the frontal bone of the lion; a similar result
was mentioned in horses,[19 ] in tigers,[31 ] and in small ruminants.[35 ] However, the frontal sinus of oxen occupies parts of the occipital, temporal, parietal
and interparietal bones.[35 ]
The bulk of the roof of the skull of the lions was formed by the parietal bones, which
had a well-developed sagittal crest. However, these bones do not form part of the
cranial cavity roof but form a part of the caudal wall of the cranium dorsally in
blackbucks,[20 ] and in oxen.[23 ]
The orbital and round foramina were united to form the foramen orbitorotundum in lions;
similar results were mentioned in blackbucks,[20 ] in oxen[23 ] and in ruminants.[36 ] However, the two foramina are separate in tigers,[18 ] and in dogs.[21 ]
The single ethmoidal foramen was present between the nasal and cranial cavities in
the lions, similar to what has been reported in horses,[19 ] blackbucks,[20 ] and in oxen[23 ] and yaks.[37 ] However, dogs have two ethmoidal foramina,[21 ] but none has been observed in camels.[22 ]
The external sagittal crest was thick and prominent in lions; a similar result was
mentioned in Felis bengalencis
[26 ] and in foxes,[38 ] while it is not prominent in brown bears.[25 ] Moreover, the zygomatic process of frontal bone is short, as mentioned in brown
bears,[25 ] while it is long in cats.[39 ] Furthermore, the median occipital crest was thick and prominent in lions, while
it is not present or not prominent in brown bears,[25 ] and in other carnivorous animals.[39 ] The jugular processes of the lion were small, similar to what has been observed
in dogs,[21 ] brown bears[25 ] and tigers,[31 ] while it is long in foxes.[38 ] The tympanic bulla of the lion was large, similar to what has been observed in blackbucks,[20 ] oxen,[23 ] dogs,[21 ] tigers,[31 ] F. bengalencis ,[26 ] and camels,[22 ] while it is small in brown bears,[27 ] and in horses.[35 ]
No particular tubercle was observed in the lion, as mentioned in tigers,[18 ] blackbucks,[20 ] and dogs,[21 ] while it is indistinct in ruminants.[36 ] The mastoid process was seen as a small nodule in the lion; a similar result was
mentioned in tigers,[18 ] while it is absent in blackbucks,[20 ] and in camels.[22 ] However, it is seen only as a roughened area in small ruminants.[35 ] On the other hand, it is well developed in dogs,[21 ] in brown bears,[25 ] in horses[35 ] and in wild cats.[38 ]
The mandibular symphysis in the lion was not ossified; a similar result was mentioned
in blackbucks,[20 ] dogs,[21 ] and in oxen,[23 ] spotted deers[40 ] and in tigers.[41 ] However, it is completely ossified in horses,[19 ] and in camels.[22 ]
In the mandible, the horizontal part of its ramus was curved slightly, so that it
did not make full contact when placed on a flat surface; the incisive part curving
upward away of the body remain lifted from the ground; a similar result was recorded
in blackbucks,[20 ] oxen[23 ] and in camels.[22 ] However, the horizontal part of the ramus of the mandible of the tiger is straight,
and it touches the surface at both sides when it is placed on a flat surface in tigers.[18 ] Moreover, the masseteric fossa was strongly excavated, with a well-developed crest,
indicating powerful mandibular adduction in lions,[28 ] while it has no depression in brown bears,[25 ] and in tigers.[41 ]
The dorsal border of the body of the mandible of the lion housed the dental alveoli
for three lower incisors and one lower canine on each side; a similar result was mentioned
in bears, lions,[1 ] tigers,[18 ] blackbucks[20 ] and in leopards.[42 ] Moreover, the molar part of the body housed the dental alveoli, two premolars, and
one molar in the lion, as mentioned in lions and bears,[1 ] while it housed three premolar teeth and three molar teeth in horses,[19 ] blackbucks,[20 ] and in oxen,[23 ] yaks[43 ] and in leopards.[44 ] There were two mental foramina on the lateral surface of the ramus; a similar result
was mentioned in leopards.[42 ] However, there is one foramen in horses,[19 ] in blackbucks,[20 ] in oxen[23 ] spotted deers,[40 ] yaks,[45 ] and in rhinoceros.[46 ] On the other hand, there are three foramina in tigers, 18 in dogs,[19 ] and in camels,[22 ] while, there are 2 to 3 mental foramina in tigers.[41 ]
