Skull Anatomy
and S. A. Rommel, eds), Vol. I, pp. 15–72. Smithsonian Institution
Press, Washington, DC.
Pabst, D. A., Rommel, S. A., and McLellan, W. A. (1998). Evolution of
thermoregulatory function in cetacean reproductive systems. In “The
Emergence of Whales” (H. Thewissen, ed.), pp. 379–397. Plenum
Press, New York, NY.
Pierard, J. (1971). Osteology and myology of the Weddell seal
Leptonychotes weddelli (Lesson, 1826). Antarctic Pinnipedia. Antarctic
Research Series 18, 53–108.
Pierard, J., and Bisaillon, A. (1978). Osteology of the Ross Seal
Ommatophoca rossi Gray, 1844. Biology of the Antarctic Seas IX,
Antarctic Research Series 31, 1–24.
Romer, A. S., and Parsons, T. S. (1986). “The Vertebrate Body,” 6th ed.
Saunders College Publishing, Philadelphia.
Rommel, S. A. (1990). The Osteology of the bottlenose dolphin. In
“The Bottlenose Dolphin” (R. Reeves, and S. Leatherwood, eds),
pp. 29–49. Academic Pr, New York.
Schmidt-Nielsen, K. (1984). “Scaling; Why is Size so Important?.”
Cambridge University Press, New York.
Strickler, T. L. (1978). Myology of the shoulder of Pontoporia blainvillei,
including a review of the literature on shoulder morphology in the
Cetacea. The American Journal of Anatomy 152(3), 419–431.
Young, J. Z. (1975). “The Life of Mammals, their anatomy and
Physiology.” Clarendon Pr, Oxford.
Skull Anatomy
SENTIEL A. ROMMEL, D. ANN PABST, AND
WILLIAM A. MCLELLAN
T
o appreciate skull anatomy, take a moment and look at your
own face in a mirror. The structures above the neck are
designed for the acquisition and initial processing of nutrients
and respiratory gases, the acquisition of sensory information about
light, sound, touch, odor, and taste, and the broadcast of information
about your own thoughts and emotions. Sensory and motor information is processed and sent from here to coordinate body functions.
Complex signals can be sent to others of our species via vocalizations
and/or the contractions of facial muscles. The head is our window
for contact, perception, and communication with our world, and
the skull provides the framework, the armature, for the head. Thus,
the skull is interesting in itself. It is also fundamentally important in
our picture of evolutionary biology. This article describes the skull
morphology of the evolutionarily diverse group of marine mammals
(Reynolds et al., 1999).
We discuss the skulls of seven different species of marine mammals: the manatee (Trichechus manatus), the harbor seal (Phoca
vitulina), the California sea lion (Zalophus californianus), the north
Atlantic right whale (Eubalaena glacialis), the bottlenose dolphin
(Tursiops truncatus), the polar bear (Ursus maritimus), and the sea
otter (Enhydra lutris). These marine mammal species were chosen,
in part, because much is known about them and they illustrate a
wide range of morphological adaptations. We use the domestic dog
(Canis familiaris) to provide a familiar reference.
I. Defining the Term “Skull”
The term “skull” is inexact. It has been used to describe the
entire skeleton of the head. It has also been used to refer to only
1033
the cranium, which is the housing for the brain and sensory organs
and the upper jaw. We use the word skull to refer to the entire head
skeleton, including the cranium and the derivatives of the first three
visceral arches, i.e., the lower jaw (or mandible) and the hyoid apparatus. The mandible and hyoid apparatus of marine mammals have
received less attention in the literature, but they are particularly
important in adaptations for feeding and in some cases hearing (see
below).
The skull acts as a mechanical foundation for the fat, muscle,
skin, vascular, and sensory structures that form the head. Thus, the
skull alone does not dictate the contours of the head (Fig. 1). For
example, odontocete cetaceans have a melon, a fatty facial pad,
the shape of which is only partly defined by the underlying bones
(Harper et al., 2008; Mead, 1975; Rommel et al., 2006). The relationships between the bones and the soft tissues of the head vary
among species, perhaps with major differences in head and skull profiles found in the sperm whales. Contrarily, the dorsal surface of the
right whale’s head follows closely that of the underlying skull, though
the right whale also has huge lower lips that follow the contour
of the upper jaw but are not predicted by the outline of the lower
jaw. The size and shape of the head may also influence the mechanics of locomotion, balance, and hearing. The completely aquatic species (cetaceans and sirenians) have shorter necks and less need for
“anti-gravitational” muscles that support the head than do terrestrial
mammals (imagine a right whale moving its head and neck around in
the air the way a sea lion does).
II. Feeding and Swallowing
The specific characteristics of a skull (including dentition) often
reflect the animal’s methods of feeding (Figs 2, 3). For example,
the “typical” heterodont dentition (Kardong, 1998) of terrestrial carnivores, such as the dog, is also found to various degrees in the seal,
sea lion, sea otter, and polar bear. Heterodonty is tooth shape differences in different parts of the mouth—incisors and canines rostrally
and cheek teeth (premolars and molars) caudally. Although each
of these tooth types may vary in shape, their definitions are specific
and are related to tooth attachment to the bones of the upper jaw
(Hildebrand, 1995). Incisors are found only in the premaxillary (incisive) bone; canines are found in the maxilla, in or very near the suture
with the premaxilla. Incisors, canines, and premolars are deciduous teeth; molars are not. Developmentally, there are two sets—milk
(or “baby”) teeth and adult teeth. Premolars erupt from the maxillary bones, they are deciduous cheek teeth that are found rostral to
the molars; molars are nondeciduous cheek teeth that erupt from the
maxillae. Each tooth shape may perform a distinct function, sort of a
“Swiss Army mouth” (Greg Early, personal communication). Incisors,
if chisel-like, are for slicing and chipping, and if pointed, for piercing.
Long, pointed canines are good for capturing and piercing. Relatively
blunt cheek teeth are good for crushing and grinding.
Teeth are also found in the lower jaw (mandible). The mandible
is made up of bilaterally paired dentary bones (Fig. 3). The rostral
ends of the two dentaries are joined by a mandibular symphysis. The
mandibular symphysis ankyloses with age in many mammals making the jaw a single compound bone; this occurs at an early age in
manatees whereas it may only fuse in very old dolphins. In contrast,
the unfused dentaries of the mysticetes may undergo complex axial
rotations, particularly while lunge-feeding in rorquals (Lambertsen,
1983).
In most mammals, each dentary has a horizontal body that
presents the teeth. In most mammals the dentary has a vertically
S
1034
Skull Anatomy
Florida manatee
Trichechus manatus latirostris
Sea otter
Enhydra lutris
Harbor seal
Phoca vitulina
Domestic dog
Canis familiaris
Polar bear
Ursus maritimus
California sea lion
Zalophus californianus
Northern right whale
Eubalaena glacialis
Bottlenose dolphin
Tursiops truncatus
Figure 1 Skulls and first two cervical vertebrae (except in the cetaceans illustrated here, in which all, partly
fused, vertebrae are fused) of a selection of marine mammals for comparison with those of the dog. Each species
is scaled so that the distances between the shoulder and the pelvis are similar; body cavities are therefore roughly
similar in length, allowing one to compare head sizes with visceral volumes among species. Note how the outline
of the head differs from the midline contour of the skull. Copyright S. A. Rommel.
Dental formula:
I 3/2, C1/1, P 3/3, M 1/2
Crushing
molars
Dental formula:
I 0/0, C 0/0, Ck 5-8/5-8
Grinding
cheek teeth
Dental formula:
I 3/2, C1/1, P 4/4, M 1/1
Shearing
molars
Dental formula:
I 3/3, C1/1, P 4/4, M 2/3
Shearing
molars
Dental formula:
I 3/3, C1/1, P 2-4/2-4, M 2/3
Shearing
molars
All teeth similar
20–26 per upper quadrant
18–24 per lower quadrant
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Grasping and/or
piercing teeth
DOG
FOOD
Dental formula:
I 3/2, C1/1, P 4/4, M 1-2/1
Shearing
molars
Sieving plates
of baleen
(Baleen extends from
upper jaw, medial and
ventral to lower jaw)
Figure 2 Feeding apparatus and typical food. Dominant tooth type is also given. Note that in manatees there
are no incisors or canines and that all the cheek teeth (C) are continuously replaced. Also note that the embryonic
teeth of the right whale have been replaced with horny plates of baleen in the upper jaw only. Copyright S. A.
Rommel.
directed ramus that projects into the temporal fossa; in dolphins,
the ramus is reduced or absent. Typically, the labial surface (lateral
aspect) of the dentary has small openings at its rostral end (mental foramina) for the blood vessels and nerves of the chin; manatee
mental foramina are relatively large.
Dentition complexity in mammals may be more indicative of
food type than is the case for many other vertebrates. The hardness
of teeth (which increases their likelihood of preservation in the fossil record) and specificity of dentition contribute significantly to our
current understanding of the ecology and evolution of different taxa.
Skull Anatomy
1035
Coronoid process
TMJ
(A)
Tympanohyal
cartilage
Ramus
Mandibular condyle
Tympanic bulla
Angular process
Stylohyal
Thyrohyal
Epihyal
Basihyal
Ceratohyal
Mental
foramina
Mandibular foramen
Mandibular
symphysis
Body
Mandibular condyle
Coronoid
process
Tympanic
TMJ
Tympano & stylohyal
cartilage
(B)
2
Angle
Ceratohyal cartilage
Thyrohyal cartilage
Body
Mandibular
symphysis
Basihyal in two positions
Mental
foramina
TMJ
Coronoid process
Tympanic bulla
Mandibular condyle
Tympanohyal
cartilage
(C)
Angular process
Stylohyal
Mental
foramina
Epihyal &
ceratohyal
cartilage
Ramus
Mandibular
foramen
Epihyal in two positions
1
Dental capsule
(with tooth buds)
Basihyal &
thyrohyal
Mandibular hiatus
Mandibular
symphysis
Body
Figure 3 Left lateral views of the dog (A), manatee (B), and dolphin (C) skull with attached hyoids and
medial views of the isolated right mandible. Bony elements of the hyoids are colored in gray excerpt where they
lie deep to the mandible. The manatee hyoid apparatus is presented in two positions to illustrate its motion
during swallowing. Muscles between the tongue and basihyal move the hyoid apparatus up and forward (position 1). Muscles between the basihyal and the sternum move the hyoid apparatus down and back (position 2
is exaggerated to illustrate the process). The joint between left and right dentaries (mandibular symphysis) is
cross-hatched. The mandibular foramen is enlarged in the manatee and greatly enlarged to form a mandibular
hiatus in the dolphin. The mandibular hiatus of the dolphin dentary is a large opening on the medial aspect
of the lower jaw. Within this hollow region there is a intramandibular fat body that extends to encompass the
ear—this fat functions as an acoustic channel for the reception of sound. TMJ temporomandibular joint.
Teeth and hyoid apparatus of the dog after Evans (1993). Copyright S. A. Rommel
Typically, deciduous teeth are replaced vertically; the developing permanent teeth are deep to the milk teeth. These teeth are
replaced only once. In contrast, manatee (but not dugong!) teeth
are continuously replaced. Manatee tooth replacement is horizontal,
beginning at the back of the tooth row (Fig. 3). This unusual method
of horizontal tooth replacement is found in only a few other mammals such as elephants and kangaroos. In addition, unusual for manatees is the lifelong generation of new tooth buds, which develop in
the dental capsule at the caudal end of each tooth row. Each manatee tooth moves forward and the roots grow in length as the crown
erupts. The crown of the tooth begins to wear as it occludes with the
opposite teeth; simultaneously, the root begins to resorb (Domning
and Hayek, 1984); the processes underlying this phenomenon are
not yet fully understood. Thus, as each manatee tooth moves forward
in the jaw, it becomes smaller at the top and bottom; when it reaches
the rostral end of the tooth row the small flattened vestige falls out.
Manatees typically do not have incisors, although small rudiments
of premaxillary incisors occasionally are observed in fetuses. Baleen
whales lose their embryonic teeth and develop baleen (Fig. 2).
Postweaning, baleen whales acquire food by sieving plankton, small
fish, and (in the case of gray whales), benthic invertebrates, using
plates of horny (keratinized) baleen suspended from their upper jaws
(Pivorunas, 1979).
In some species, all of the teeth have the same shape—this is
the homodont condition. The homodont dentitions of odontocetes
and manatees differ in shape and function (they are single-rooted,
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1036
Skull Anatomy
External bony naris
Nasal
Maxilla
Occipital Zygomatic arch
Mandibular ‘fossa’
O – orbit, TF – temporal fossa, IF – infraorbital foramen, POF –
postorbital process of the frontal, EAM - external acoustic meatus
POF
Occipital condyles
(& foramen magnum)
Nasal
POF
TF
TF
O
O
TF
O
IF
IF
EAM
EAM
IF
EAM
POF
POF
O
O
POF
TF
TF
TF
O
IF
IF
EAM
IF
EAM
EAM
IF
TF
TF
O
IF
POF
EAM
O
EAM
POF
Figure 4 Selected bony features of the cranium. The rostrum, composed of the premaxilla, maxilla, and occasionally the nasal, forms the “face” or muzzle of each species. The zygomatic arch, which supports the masseter muscles, may be composed of a single bone (the jugal) or parts of as many as three bones in some species.
Arrows indicate directions of air flow at the external bony nares, vertebral column articulation at the occipital
condyles, and lower jaw articulation at the mandibular fossa; note that the mandibular fossa of the manatee
includes a convex tubercle. Postorbital processes of the frontal may be present; it is absent in the seal, small in
the sea otter, and relatively large in the dolphin and right whale. The region spanned by the tympanic membrane is visible in manatees but hidden within the middle ear of the other species. Copyright S. A. Rommel.
S
conical, grasping teeth for dolphins and multi-rooted, multi-cusped,
grinding teeth for manatees).
The dental formula is an alphanumeric abbreviation for the adult
numbers of incisor, canine, premolar, and molar teeth—the number
of each tooth type in the upper and lower half of the jaw (Fig. 2).
For example, I 3/2, C1/1, P 3/3, M 1/2 describes the dentition of
the sea otter. Thus, the adult sea otter has 3 incisors on each side of
the upper jaw and 2 incisors on each side of the lower jaw, etc. The
lower jaw generally mirrors some of the features of the upper jaw,
particularly the dentition (Figs. 2, 3).
Feeding habits may also be reflected in the shapes of the rostrum,
the zygomatic arch, and the temporal fossa (Fig. 4). Relatively large
temporal muscles and their fossae are typical of carnivorous mammals
that tear or shear flesh without finely dividing it in the mouth, and/
or have teeth for killing and temporarily holding prey (Hildebrand,
1995). Carnivorous mammals have upper and lower tooth rows that
have little or no horizontal motion but rather occlude with a chopping motion, using a simple hinge joint. Their temporomandibular joint or TMJ is roughly in line with the tooth row. In contrast,
the TMJ in herbivores is typically above the tooth line (Figs 2, 3).
Relatively large masseter muscles, and robust zygomatic arches that
support them, are more typical of herbivorous mammals that use
a crushing and rolling action to chew. This feeding style requires a
TMJ that can slide horizontally and a large masseter to apply force
along the cheek tooth row. Thus, the shape of the TMJ also reflects
feeding habits. In carnivores a dorsally-convex mandibular condyle of the dentary bone fits into a distinct, ventrally-concave fossa
of the squamosal bone (Figs 3, 4). In herbivores, the TMJ shape is
more complex than that of the carnivores. In some ungulates such
as the horse and pig, there is a distinct squamosal articular tubercle
(tuberculum articulare) that articulates with the mandibular condyle
(Nickel et al., 1986; Popesko, 1979).
TMJs of sea otters, seals, sea lions, and polar bears are mechanically constrained, allowing up and down movement but little or no
transverse motion of the lower jaw. Of the skulls illustrated, the mandibular fossa of the otter is the most restrictive with a deep concavity that grips the mandibular condyle (in some cleaned skulls the
mandible cannot be removed with out damaging the margins of the
mandibular fossae). The mandibular fossae of the seal, sea lion, and
polar bear are shallower, and more similar to that of the dog. The
TMJs of odontocete cetaceans appear to be mechanically less constrained because of their relatively large radii of curvature. Live dolphins, however, exhibit simple up-and-down (opening-and-closing)
jaw movements similar to those observed in the dog. As mentioned
above, odontocetes have simple fish-and-squid-grasping teeth. The
TMJs of rorquals are relatively unconstrained; they can move up and
down, forward and back, and rotate along the long axis of the dentary.
These relatively unconstrained joints are tough and pliable fibrous
Skull Anatomy
structures that can absorb the mechanical shock associated with lunge
feeding. Rorqual lower jaws must support the large, pleated gular
sac into which flows a large volume of water and prey during lunge
feeding. Gular sac contraction forces water out through the relatively
short baleen plates trapping the prey (Lambertsen, 1983; Pivorunas,
1979). Right whale TMJs restrict jaw movements to up and down and
rotation of the mandible along its long axis (Werth, 2004). The jaws
of these skimmers support massive lower lips that guide an almost
continuous stream of water past long baleen plates (Pivorunas, 1979;
Werth, 2004). Gray whales, which are bottom feeders, have relatively
robust lower jaws. The mandibular condyles of manatees are slightly
flattened sub-cylinders that articulate with a distinct articular tubercle, which is located rostral to the shallow mandibular fossa (Fig. 3).
Manatees must have a relatively mobile TMJ to accommodate grinding their food. The motions of the manatee TMJ include influence
of the robust pterygoid process as a pivot, creating a slightly arched
transverse travel of the occluding tooth rows. These motions, which
include lateral and a small amount of rostral motion, provide the
action required for grinding vegetation as well as stimulating the rostral migration of the teeth (Domning, 1978).
The shapes of the dentaries of the three marine mammals that
are illustrated in Fig. 3 are dramatically different—that of the dog
is roughly similar to those of the sea otter, seal, sea lion, and polar
bear (Fig. 1). Note the angular process in these latter species; it is
located ventrocaudal to the TMJ—that of the polar bear is much
more pronounced than those of the other marine mammals. The
dolphin dentary is elongate with a reduced ramus and a very small
angular process. The manatee dentary has a forward-directed, robust
coronoid process and a relatively flat mandibular condyle; there is no
discernable angular process.
Feeding includes swallowing. Chewing involves positioning of the
food between the teeth by the tongue; swallowing requires the coordinated action of these muscles and bones as food leaves the oral cavity and moves through the pharynx. How do the bones of the head
accommodate swallowing? The hyoid apparatus is an important structure in both feeding and swallowing (Fig. 3); it is a complex of hinged
bony and cartilaginous elements that are suspended from the ventral
aspect of the cranium and lie between the dentaries. The hyoid bones
(labeled with the suffix -hyal to minimize confusion with hyoid muscles, Reidenberg and Laitman, 1994), provide the mechanical support of many of the muscles that act upon the tongue and the larynx.
Muscles between the tongue and basihyal move the hyoid apparatus
up and forward. Muscles between the basihyal and the sternum move
the hyoid apparatus down and back (Fig. 3). The tongue may also help
exclude water from food that is swallowed under water.
In most mammals, the hyoid apparatus is attached to the ventral
skull at one of the bony elements of the compound temporal bone, at
or near the external auditory meatus (Figs 3, 4): in carnivores via the
mastoid process of the periotic bone; in man, ruminants, and horses
via the styloid process of the tympanic bone; and in the pig via the
nuchal process of the squamosal bone (Nickel et al., 1986). The seal,
sea lion, and sea otter all have hyoid apparatuses that are similar in
configuration and attachment to that of the dog. The dolphin and
manatee have relatively robust hyoid apparatuses when compared to
the other marine mammals. In suction feeders, such as the squideating beaked whales, pilot whales, and kogiids, the hyoid apparatus and its associated muscles are massive (Reidenberg and Laitman,
1994). In contrast to most other mammals, the manatee and the
dolphin hyoid apparatus is attached to the ventral skull at the paracondylar (paroccipital) processes of the exoccipital bones (see below)
in a position caudolateral to the tympanoperiotic complex. There are
1037
distinct concavities for hyoid attachment in the paracondylar processes (Fraser and Purves, 1960). This attachment helps acoustically
isolate the hyoid apparatus from the bones of the tympanoperiotic
complex, which are themselves not fused to the rest of the cranium
(see below). Interestingly, in the live dolphin there is an air sinus
(posterior sinus) at the rostral aspect of the concavity, between the
hyoid attachment and the tympanoperiotic (Fraser and Purves,
1960), which would add to the mechanical isolation. In some odontocetes (i.e., Kogia, Ziphius) there are large, well-developed mastoid
process of the tympanoperiotic. These mastoid processes are similar in position to the paracondylar process of the dolphin. There are
no deep concavities on these mastoid processes but there are similar
but shallow regions, medial to the jugular notches, on the caudolateral margins of the relatively thick crests of the basiocciptal bones.
III. Bony Features and Bones
One approach to studying the skull is to focus on a few specialized bony features (Fig. 4). Bony features are morphological characters or landmarks that make up one or more bones. Size, shape, and
positions of bony features reflect evolutionary, developmental, and
mechanical pressures in a grossly visible manner. For example, the
zygomatic arch, which supports the masseter muscle that helps close
the jaws, may be composed of one, two, or three bones depending
on the species. The rostrum or muzzle may be elongate and may or
may not include the nasal bones. Thus, to characterize individual
skulls without having to identify individual bones, biologists use the
morphology of bony features such as the postorbital processes; zygomatic arch shape and composition; rostrum length; orbit size, shape,
and position; and jaw articulation.
In general, large, forward-facing orbits are characteristic of predators
that rely on vision as their primary sensory modality, whereas laterally
facing orbits are more typical of non-predatory species (Hildebrand,
1995). Also note that the orbits of most species in Fig. 4 are open caudally (having small postorbital processes), in contrast to those of the fully
aquatic mammals. In the species in which the orbit is open, there is a
postorbital ligament caudal to the eye that extends between the ventrally
projecting postorbital process of the frontal bone and a dorsally projecting postorbital process of the jugal and or the squamosal bones (a bony
feature on the dorsal aspect of the zygomatic arch); these postorbital
processes are prominent in the polar bear.
In all species, the external bony nares are bordered by the nasal
bones. The positions, relative to the rostrum and braincase, of the
external bony nares may reflect respiratory adaptations to diving,
feeding, and locomotion. The occipital condyles position the head on
the neck and influence the flexibility of this joint (Figs. 1, 2). Some
marine mammal species have short necks, placing the base of the
skull very near the shoulder joint and the thoracic cavity. Species
with long necks may have a wide range of neutral head positions and
may also have a greater range of movement than the fully aquatic
species (King, 1983). In most mammals the joint between occipital
condyles and the first cervical vertebra (atlas) is restricted to two
degrees of mechanical freedom; an additional degree of freedom is
acquired with the rotation between the atlas and axis vertebrae. In
cetaceans with fused cervical vertebrae three degrees of freedom are
potentially available in the joint between the condyles and the atlas.
IV. Ground Plan of the Skull Bones
What other factors shape the skull? In all vertebrates, the skull
bones develop from ossification centers in a basic pattern that partially or completely encloses the brain and encapsulates the sensory
S
1038
Skull Anatomy
Frontal sinus
Cranial cavity
Cranial cavity
Choana
Nasal bone
C6
Choana
Axis, C2
Naris
Naris
Tongue
Trachea
Epiglottis
Soft palate
C7
Hard palate
Rim of choana
Soft palate
Epiglottis
Trachea
Axis, C2
Nasal bone
Tongue
Hard palate
Rim of choana
Air
Nasal cavity
Esophagus
Food
Trachea
Air
Palate
Food
Oral cavity
Epiglottis positions
Cut bone, hard palate
Epiglottal cartilage, nasal bone
Soft palate
Bony nasal passage (choana)
Nasal bone
Cranial cavity
Blowhole
Diverticulum
Air
Atlas-axis, C1-C2
Melon
C7
Esophagus
Food
Food
Oral cavity
Tongue
Trachea
Air
Epiglottis (goose beak)
Hard palate
Rim of choana
Soft palate
Figure 5 Comparisons of the morphological adaptations of the mammalian head that allow respiration while
food is in the mouth. Separation of oral and nasal cavities accommodates prolonged chewing and allows teeth to
be modified accordingly. The dog and manatee are schematically represented in the upper panel. In the dolphin
(lower panel) further modification is shown to accommodate the migration of the respiratory opening to the top of
the head. Copyright S. A. Rommel.
Cartilaginous neurocranium
later in development
Cartilaginous neurocranium
earlier in development
Cartilage
Nerve tissue
Olfactory sac
n. I
Olfactory lobe
Lens
Retina
n. II
Ossification centers
Otocyst
n. VIII
Spinal cord
S
Ossification centers in the
cartilaginous neurocranium
Ethmoid
Olfactory capsule
Orbitosphenoid
Optic capsule
Presphenoid
Prechordal cartilage
Parachordal cartilage
Brain “capsule”
(Cartilagenous
neurocranium)
Otic capsule
Basisphenoid
Otic (peri-otic)
Basioccipital
Exoccipital
Figure 6 Schematic illustration of ventral views of the developing vertebrate skull. Modified after Kent and Miller (1997). The
basic plan of encapsulation of the senses and brain is illustrated in the left two drawings. The right drawing illustrates the ossification centers that will eventually become the replacement bones of the cranium.
organs of olfaction, vision, hearing, and balance (Fig. 6). Tissues that
are preformed in cartilage and that eventually develop into bone are
referred to as endochondral or replacement bones (these form the
chondrocranium); those tissues deposited directly as bone within
specialized connective tissue membranes are referred to as dermal or
membrane bones (these form the dermatocranium). The distinction
between endochondral and dermal bones is valuable in establishing
homologies with skull bones of the lower vertebrates; however, once
bony tissues are formed, the two kinds of bone are indistinguishable
microscopically (Nickel et al., 1986).
How does one determine which bones of the skull are homologous between species? A systematic but simplified approach that
allows one to compare homologous elements is to utilize a generalized schematic skull (Fig. 7). This schematic is a particularly useful
way to avoid the “mental indigestion” of having to memorize all the
individual bones in several species (Romer and Parsons, 1977).
Skull Anatomy
Parietal, Par
Frontal, Frn
Orbitosphenoid, Osp*
1039
Alisphenoid, Als*
Interparietal, Int
Cribriform plate, Crb*
Supraoccipital, Soc*
Nasoturbinate, nTur
Periotic, Per*
Ethmoid, Eth*
Exoccipital, Exo*
Nasal, Nas
Tympanic, Tym
Lacrimal, Lac
Basioccipital, Boc*
Tympanohyal, tHyo*
Ethmoturbinate, eTur
Presphenoid, Psp*
Stylohyal, sHyo*
Epihyal, eHyo*
Thryohyal, tHyo*
Basihyal, bHyo*
Vomer, Vom
Maxilloturbinate, mTur
Premaxilla, Pmx
Ceratohyal, cHyo*
Squamosal, Sqa
Basisphenoid, Bsp*
Pterygoid, Pty
Maxilla, Max
Dentary, Den
Jugal, Jug
Palatine, Pal
Figure 7 Left lateral schematic of the mammalian skull illustrating relative bone positions. Most skull bones
are bilaterally paired. This schematic approach has been used for more than 100 years and provides a framework in which to compare a wide variety of mammalian skulls. Modified after Flower (1885), Kent and Miller
(1997), and Evans (1993). Recall that the nose, eyes, and ears are encapsulated early in development; these
three sensory areas are represented by circular regions in the schematic. Endochondral bones are indicated
with an asterisk. Copyright S. A. Rommel.
In some species, individual bones fuse (ankylose) to form compound bones1; these include the occipital, temporal, and sphenoid
“bones.” Of particular interest is the temporal “bone,” which is made
up of many separate bony elements and/or ossification centers (Kent
and Miller, 1997). These separate bones include the squamosal, the
periotic, the tympanic, the middle ear ossicles, and in some species a distinct mastoid. In many mammals, once skeletal maturity is
reached, the bulk of each temporal is a single unit with no visible
sutures between the bony elements. Thus, it is common with terrestrial mammals to refer to the temporal as a single bone, but this is
inappropriate for several of the marine mammals, particularly some
of the cetaceans and the sirenians because the earbone complex
(periotic and tympanic) do not ankylose to the rest of the skull.
The exploded diagram of the cranium of the Florida manatee
illustrates how some bones fit together simply whereas in other
places they overlap (Fig. 8). The compound occipital bone, which
forms a ring around the foramen magnum, is composed of the basioccipital, exoccipitals, and supraoccipital (Jollie, 1973; Kellogg, 1928;
Romer and Parsons, 1977).
Figure 9 is a left lateral view of the individual cranial bones for
our representative marine mammals. Contrast this illustration with
Fig. 4 to reinforce the distinction between bones and bony features;
see Fig. 1 to compare skull size to total body size.
1
We have used three different terms incorporating the word “bone”.
Bones are discrete ossifications that can be traced phylogenetically.
Compound bones are structures that appear to be single units in adults
of some species because the joints between the component bones have
been resorbed or are not apparent. Bony features are gross features, such
as the zygomatic arch, that are made up of discrete and distinct bones or
parts of bones (e.g., the zygomatic process of the squamosal bone).
V. Cranial Joints
Skull bones can meet in several ways and attach to each
other by more than one type of material (e.g., cartilage and other connective tissue). Joints between adjacent cranial bones are referred to
as sutures or synchondroses. Sutures are fibrous joints between dermal bones; synchondroses are cartilaginous joints between endochondral bones. Sutures and synchondroses are regions of growth between
individual bones; in adults they may also function to relieve stresses
that are produced in the skull (Gordon, 1988). At parturition, some
joints provide the flexibility for a relatively large brain within the cranium to pass through a relatively narrow birth canal. In the illustration
of the exploded manatee cranium (Fig. 8), the hatched regions represent (Fig. 9) joints or regions of overlap. In Fig. 10, some of the joints
of the dog skull are compared with those of the manatee and dolphin
skull. The type of joint generally reflects the mechanical forces acting
on the adjacent bones. Different types of joint may be found between
the same bones in different species; types may also be different in different parts of the same joint, probably to reflect differences in forces.
Interlocking joints can absorb mechanical energy. Movable joints
eliminate shearing forces. Butt joints can support little shear but are
strong in compression. Squamosal or scarf joints allow more surface
contact between adjacent bones and are stronger than simple butt
joints. Some bone configurations affect the complexity of joints, and
this complexity, in turn, affects the action and strength of the joints.
Relative aging of skulls may be determined by evaluating the sequence
of ankyloses of sutures and synchondroses, unfortunately few systematic studies have been completed (Moore, 1981).
VI. Foramina
The development of the skull bones proceeds at a pace different
from that of the soft tissues of the head. Bone is constantly being
S
1040
Skull Anatomy
Nasal, Nas
Parietal, Par
Frontal, Frn
Overlapping sutures
Supraoccipital, Soc
Premaxilla, Pmx
Lacrimal, Lac
Exoccipital, Exo
Basioccipital, Boc
Rommel 08
Periotic, Per
Jugal, Jug
Malleus, Mal
Squamosal, Sqa
Tympanic, Tym
Maxilla, Max
Basisphenoid, Bsp
Alisphenoid, Als
Orbitosphenoid, Osp
Pterygoid, Pty
Palatine, Pal
Figure 8 Left lateral view of an exploded cranium of the Florida manatee. This figure illustrates the overlapping and/or abutting margins of bones that make up the sutures and synchondroses of the cranium. Copyright
S. A. Rommel.
Frn Jug
Par
Lac
Lac
Nas
Max
Frn Osp* Par Soc*
Pmx
Soc*
Sqa
Exo*
Jug
Pmx
Max Pal
Als*
Exo*
Pal Pty Sqa
Tym Boc*
Max
Bsp
Pty
Frn
Nas
Lac
Frn Jug Osp* Sqa
Pmx
Exo*
Max Pal Als*
Pty Tym
Nas
Max
Pmx
S
Exo*
Max Jug
Pty Pal
Osp*
Jug
Pty
Pal
Als*
Soc*
Soc*
Sqa
Par
Sqa
Max
Exo*
Lac
Als*
Exo*
Frn
Pmx
Osp* Pty
Soc*
Tym
Sqa
Nas
Pal Jug
Par
Max Vom Pal Pty Sqa Tym
Frn
Max
Frn Jug
Exo*
Boc*
Par
Pmx
Lac
Boc*
Als* Tym
Pmx
Max
Frn
Soc*
Pmx
Soc*
Pmx
Boc*
Sqa
Nas
Lac
Nas
Soc*
Boc*
Tym
Osp* Par
Lac* Frn
Osp* Par
Pal
Par
Nas
Per*
Boc*
Tym
Jug
Exo*
Boc*
Pal
Tym
Sqa
Figure 9 Left lateral illustrations of individual cranial bones of selected marine mammals and the dog.
Abbreviations are the same as in Figs. 7 and 8. Use Figure 8 to help visualize how the basic plan of mammalian skull
morphology is modified in each species. Endochondral bones are indicated with an asterisk. Copyright S. A. Rommel.
remodeled; this takes place at the level of the individual during its
lifetime in response to trauma, nutrition, and localized conditions.
Remodeling also takes place at the population level over longer time
spans and thus can indicate evolutionary processes. This plasticity is
reflected in the way individual skull bones form around vessels and
nerves. The resulting openings, or foramina (singular, foramen), are
often phylogenetically conserved and so can be used to establish
homologies of the same bones across different species. An individual
Skull Anatomy
FOL
SQA
PLA
PLA
SYN
SER
FOL
SER
SQA
1041
Cartilage
SQA
SER
SQA
PLA
PLA
SYN
PLA
SER
SER
FOL
SER
FOL
FOL
SQA
SQA
SQA
SQA
SER
PLA
SYN
PLA
SER
FOL
PLA
SER
PLA
SYN
FOL
SYN
(A)
cut bones
(B)
FOL
SYN
(C)
SYN
SYN
Figure 10 Joint types in the cranium of the dog (A), manatee (B), and dolphin (C). Sutures are fibrous joints
between dermal bones; synchondroses are cartilaginous joints between endochondral bones. Joints allow growth
of adjacent bones, provide limited flexibility and absorb mechanical forces. Suture types are defined by their
shape. PLA, plane or butt joint (harmonious suture, sutura plana)—an approximately straight suture with
nearly squared-off margins. SQA, squamous or scarf joint (sutura squamosa)—a suture with tapered overlapping margins. FOL, foliate joint (sutura foliata)—a regular suture with small alternating vertical bony plates, in
which adjoining bones interleave. SER, serrate joint (sutura serrata)—an irregular suture, in which adjoining
bones interlock. A synchondrosis (synchondroses cranii), SYN, has persistent cartilage between bones. Below,
simplified, sagittally sectioned crania illustrate those joints that can be observed on the midline. Definitions are
from a variety of sources; parenthetical names are from Schaller (1992). Copyright S. A. Rommel.
nerve or blood vessel may be completely surrounded by a bone or
bones of the skull, resulting in a specific foramen. Because this process occurs early in the development of the individual and appears to
be similar in all vertebrates, we use cranial nerve foramina to help us
identify the skull bones (Figs 11, 12).
In some species, or even in individuals of the same species of different ages, instead of a single foramen for each individual nerve,
one or more nerves may exit the braincase through a single opening. Some openings are very large and irregular and are referred to
as hiatuses (Fig. 12). The cranial hiatus of the dolphin (Fraser and
Purves, 1960) and manatee may include the following nerve openings: optic foramen, orbital fissure (anterior lacerate foramen), and
oval foramen—plus the openings for vessels between the last two.
The cranial hiatus is not present in the other marine mammals
because their skulls have earbone complexes that are firmly attached
to the other bones of the skull (see the compound temporal bone
above). The tympanic and periotic bones are often referred to as the
earbone complex or the tympano-periotic complex. The earbone
complexes of the manatee and dolphin have loose connections with
the rest of the skull bones, presumably to produce an acoustic isolation from the rest of the skull; in cleaned skulls the earbone complexes may fall out of the skull in these taxa. In life, the odontocete
tympanoperiotic is surrounded by peribullar sinuses that add to this
acoustic isolation (Fraser and Purves, 1960; Houser et al., 2004). The
cranial hiatus includes the petrooccipital fissure, which is an irregular opening between the tympanic and periotic bones (housing the
ear) and the alisphenoid, basisphenoid, basioccipital, and exoccipital
bones of skull base (Nickel et al., 1986; Schaller, 1992). In the terrestrial mammals, the margins of the petrooccipital fissure may join
to form one or several foramina (foramen ovale, jugular foramen,
carotid foramen, hypoglossal foramen, caudal lacerated foramen).
The mandible also has a number of foramina. At its caudal end,
the medial aspect (lingual surface) of the dentary has a mandibular
foramen, which is the opening of the mandibular canal for the alveolar vessels and nerves. In manatees, the mandibular foramen is relatively large because of the large amount of soft tissues and perioral
bristles of the chin supplied and innervated via the mandibular canal.
In dolphins, the mandibular foramen is even larger; it is referred to
as a hiatus (Fraser and Purves, 1960). The odontocete dentary is
almost hollow and is filled with a well-vascularized mandibular fat
body, which performs the acoustic function of receiving and guiding
sound energy to the earbones (Norris and Harvey, 1974; Koopman
et al., 2006).
In some cetaceans (e.g., Kogia, Ziphius) the internal auditory meatus is a long narrow canal (Fig. 13) (Rommel et al., 2006).
Interestingly, as mentioned above, these cetaceans have distinct mastoid bones. Fraser and Purves (1960) describe secondary growth of
the basioccipital, parietal, and squamosal bones around the margins
S
1042
Skull Anatomy
Vmn
Foramen
ovale
Vmx
Foramen
rotundum
Brain
case
Orbit
I
Cribriform
plate
VII
Stylomastoid
foramen
XII
Hypoglossal
foramen
Nasal
capsule
II
Optic
foramen
III,IV
Vo,VI
Orbital
fissure
Ear
capsule
IX,X,XI
Jugular
foramen
Figure 11 Left lateral schematic of openings, or foramina of the
skull. Foramina can be used to establish homologies of the same
bones in different species; each foramen associated with one or more
of the 12 cranial nerves (labeled I through XII) has a name that is
used (fairly) consistently by vertebrate morphologists. Thus the cribriform plate, found at the rostral margin of the braincase, is associated with the olfactory nerves (this will be parenthetically referred
to as I-olfactory n.) in all of the species that have a sense of smell
(even odontocetes, which do not have olfactory nerves as adults, have
these perforations (Rommel, 1990). The second cranial nerve passes
through the optic foramen and usually perforates the orbitosphenoid
bone (II-optic n.). The orbital fissure is usually at the orbitosphenoid
bone-alisphenoid bone suture (also anterior lacerate foramen; III-oculomotor n., IV-trochlear n., Vo-ophthalmic branch of trigeminal n.,
VI-abducens n.). The foramen rotundum (Vmx-maxillary branch of
the trigeminal n.) and the foramen ovale (Vmn-mandibular branch
of the trigeminal n.) perforate the alisphenoid bone. The stylomastoid foramen is located at the tympanic bone-basioccipital bone
suture (VII-facial n.). (Nerve VIII-vestibulocochlear n. is not shown;
it perforates the periotic bone through its internal auditory meatus.) The jugular foramen (also caudal lacerate foramen) is at the
exoccipital bone-basioccipital bone suture (IX-glossopharyngeal n.,
X-vagus n., XI-accessory n.). The hypoglossal foramen usually perforates the exoccipital (XII-hypoglossal n.). An additional cranial nerve
(O-terminal n.) was discovered after the numbering system was
developed. This nerve is found rostral to the olfactory nerve; it has
been described only (of the species illustrated) in the odontocetes and
is not illustrated here. Copyright S. A. Rommel.
of the cranial hiatus, which narrows and elongates the channels for
the facial and acoustic nerves.
VII. Skull Cavities
S
The cranial cavity (Figs 5 and 13) houses the brain, its meninges, and its vasculature (Nickel et al., 1986, Romer and Parsons,
1977). The roof (calvarium) and lateral walls of the braincase are
typically made up of the frontal and parietal bones with the caudal
wall formed by the supraoccipital and exoccipitals (Figs 7, 8, and 9).
Rostrally, there is the ethmoid bone with its perforated cribriform
plate, medial extensions of the inner lamina of the frontal bone, and
portions of the sphenoids (see below). In odontocetes lateral wings
of the vomer also contributes to the rostral wall of the cranial cavity.
The floor of the cranial cavity is formed by the basioccipital, the
basisphenoid (including the depression for the pituitary) with its lateral
wings (the alisphenoids), and the presphenoid with its lateral wings
(the orbitosphenoids) (Figs 7, and 12). The alisphenoid and orbitosphenoid wings extend dorsolaterally between the more dorsal skull
bones in a wide variety of shapes and sizes—these two winged bones
(collectively called the sphenoid bone) have most of the foramina for
the cranial nerves and may be the most variable and difficult to recognize in different taxa (Figs 7, 9, and 11).
The nasal cavity is separated from the oral cavity by the secondary
palate. The secondary palate is formed by the hard and soft palates
(Fig. 5). The secondary palate makes a very important contribution
to the evolutionary forces that shaped mammal skulls as it allows prolonged chewing while breathing, providing additional time for food
processing in the mouth. The nasal cavity extends from the external
bony nares to the perpendicular plate of the ethmoid bone. The nasal
cavity is typically a roughly tubular structure that occupies the entire
length of the rostrum of the skull in most mammals, but not in cetaceans. In some terrestrial species, it may be paralleled on either side
by enclosed maxillary sinuses. The bony supports for the nasal cavity
are formed by the premaxillae, maxillae, frontals, vomer, palatines, and
in some species the lacrimals and jugals (Nickel et al., 1986; Romer
and Parsons, 1977). There is often a dorsoventral medial nasal septum in the nasal cavity; it is formed by cartilage rostrally and by a bony
extension of the ethmoid caudally. The vomer (an unpaired, relatively
thin, ventral midline bone) may also contribute to the ventrolateral
aspects of the nasal septum.
The nasal septum divides the nasal cavity into separate left and
right air channels called choanae (Fig. 5). Caudally, the choanae may
lose their septum near the junction of the soft and hard palates (rim
of the choanae; Figs 5 and 12). In many species, a thin layer of the
vomer extends caudally along the ventral midline to cover the ventral
aspects of the presphenoid and basisphenoid as the animal ages. In
some mammals, particularly dolphins, this portion of the thin vomer
is often fenestrated, exposing the synchondrosis between the basisphenoid and presphenoid bones (Fig. 12).
Conchae (turbinates, turbinals) are thin lamellae of bone (covered with mucous membrane in life) that project into the nasal cavity. Conchae increase the surface area in the nasal cavity for heat
exchange, water balance, and olfaction (Moore, 1981). The more
rostral conchae develop as outgrowths of the maxillae and nasals, the
more caudal chonchae develop from the ethmoid bones (Nickel et al.,
1986). In stark contrast to most other mammals, the nasal cavities of
cetacea are not part of the rostrum. Instead, cetacean nasal cavities
are almost vertical channels just rostral to the braincase (see telescoping below) and are devoid of conchae; the bones dividing and bordering the nasal cavity are displaced by the vomer and the pterygoid
(Mead and Fordyce, 2008; Rommel, 1990). This helps allow for the
rapid respiratory cycle of cetaceans (Pabst et al., 1999). The conchae
of sea otters, sea lions, and seals are very convoluted, almost filling the
nasal cavity with lace-like networks of bone. These structures significantly increase in surface area and have been shown to be important
for water and heat conservation in seals and sea otters (Folkow et al.,
1988; Huntley et al., 1984).
Skull bones of most mammals are mechanical marvels. Only relatively recently in engineering history has man built composite structures (monocoques) that approach the efficiency of design found in
the mammalian skull (Gordon, 1988). In many species, some of the
skull bones are made up of a layer of spongy bone (diploe) and/or
air-filled sinuses (Fig. 5) sandwiched between two thin “panels” of
rigid cortical bone commonly referred to as the internal and external
laminae (singular lamina) (Nickel et al., 1986; Schaller, 1992). This
excavation of sinuses within bones is called pneumatization (Nickel
et al., 1986). The resulting multilayered structure is strong, yet has
Skull Anatomy
Pmx
1043
Pmx
Vestigial alveolus
Incisive for.
Antorbital notch
Max
Major palatine for.
Vom
Lamalle of Pty sinus
Antorbital notch
Pal
Infraorbital for.
Zygomatic proc., Max
Max
Pty
Pal
Sqa
Vom
Als
Rim of L choana
Orbital fis. (II-VI)
Pterygoid proc., Pal
Pterygoid proc., Pty
Mandibular ‘fossa’
Postglenoid proc.
Cranial hiatus (V3, IX-XII)
Paracondylar proc., Exo
Hypoglossal for. (inconstant)
Occipital condyle
for. magnum
Boc
Pty
Tym
Bsp
Exo
Boc
Vent. infraorbital for.
Supraorbital proc., Frn
Rim of L choana
Orbital fis. (II-VI)
Lac
Jug
Jug
Frn
Osp
Vom
Bsp
Par
Sqa
Als
Tym
Exo
Boc
Pty crest
Foramen ovale (V3)
Mandibular fos.
Postglenoid proc.
Cranial hiatus (IX-XI)
Paracondylar proc., Exo
Jugular notch
Hypoglossal for. (XII)
Boc crest
for. magnum
(B)
(A)
Pmx
Max
Pal
Jug
Incisive for.
Major palatine for.
Rim of L choana
Zygomatic proc., Max
Postorbital proc., Frn
Optic for. (II)
Orbital fis. (III-VI)
Psp
Osp
For. rotundum (V2)
Pty
Caud alar for.
Als
Mandibular fos.
Sqa
Postglenoid proc.
for. ovale (V3)
Bsp
Stylomastoid for. (VII)
Tym
Paracondylar proc., Exo
Boc
Jugular for. (IX-XI)
Exo
Hypoglossal for. (XII)
for. magnum
Vom
(C)
Figure 12 Comparison of the basicranial morphology of the manatee, dolphin, and dog. The base of the skull
has important morphological features that help with keying out different species. Note the large opening (cranial
hiatus), which is illustrated for the manatee and dolphin; it is not present in the other marine mammals because
their skulls have earbone complexes that are firmly attached to the other bones of the skull. The earbone complexes
of the manatee and dolphin have loose connections with the rest of the skull bones as part of their acoustic isolation
from the rest of the skull. The following abbreviations are used: for, foramen; fis, fissure; fos, fossa; proc, process;
L, left; R, right. Roman numerals denote cranial nerves. Fenestrations may occur in the vomer ventral to the joint
between the basisphenoid and basioccipital bones; these fenestrations make the margins of these bones and this
suture visible through the vomer. Copyright S. A. Rommel.
less weight than other bony structures. In the skull bones of most
placental mammals, pneumatized paranasal sinuses develop embryonically as invaginations from the adjacent air spaces. These sinuses
vary considerably even within species; they become larger and more
numerous as the individual ages (Moore, 1981). In many species,
paranasal sinuses help form three-dimensional bracing systems by
minimizing the mass of bone that provides the framework needed for
mechanical support of different parts of the head2. Some paranasal
2
Similar bracing systems are found in the wings and fuselages of
aircraft and the hulls of large ships (Gordon 1988).
sinuses increase the available surface area for olfactory epithelium to
detect odors (Nickel et al., 1986). Sinuses that are well vascularized
may help provide evaporative cooling (Schaller, 1992). In terrestrial
mammals, paranasal sinuses may also act as resonators that modify
sounds generated by the individual (Moore, 1981). Paranasal sinuses
occur in the frontal (Fig. 5) and maxillary bones of the dog and in the
frontal, ethmoid, and presphenoid bones of man; in other terrestrial
mammals they also occur in the exoccipital, jugal, lacrimal, nasal,
palatine, parietal, basisphenoid, and vomer (Moore, 1981; Nickel
et al., 1986; Schaller, 1992).
In contrast to most other mammal skulls, manatee skull bones
are thick and made of almost solid amedullary bone (Fawcett, 1942).
S
1044
Skull Anatomy
Supraoccipital
Parietal
Cranial cavity
Long narrow channels
for cranial nerves
VII & VIII
Cranial
hiatus
Squamosal
Tympanoperiotic
Basioccipital
crest
(A)
(B)
Figure 13 Cross sections of the skulls of Tursiops (A) and Ziphius (B). The cross sections (at the level
of the ear) are scaled to have similar areas of braincase. In Tursiops, the pathway out of the braincase for
cranial nerves VII and VIII is a short open cranial hiatus bordered by relatively thin bones, whereas in
Ziphius it is a narrow, relatively long channel. The ziphiid basioccipital bones are relatively massive with
thick ventrolateral crests; in contrast, delphinid basioccipital bones are relatively long and tall, but thin
and laterally cupped. Note that in contrast to the Ziphius calf cross section, the adult head would have a
greater amount of bone and the brain size would be relatively smaller. Modified from Rommel et al. (2006).
(A)
External
nares
Nasal bones
External
nares
Temporal
fossa
Maxillary bones
Temporal
fossa
Occipital bones
(B)
Orbit
S
Orbit
Nasals
Max & Pmx
Max & Pmx
Max & Pmx
(C)
Max & Pmx
Soc
Max only
Orbit
Brain
Nasals
Soc
Brain
Orbit
Max only
Figure 14 Dorsal (A), lateral (B), and schematic (C) views illustrating telescoping in odontocetes (left, e.g., Tursiops)
and mysticetes (right, e.g., Eubalaena). Telescoping refers to the elongation of the rostral elements [both fore and after
in the case of the premaxillary and maxillary bones (Pmx and Max), the vomer, and mesorostral cartilage], the dorsorostral movement of the caudal elements [particularly the supraoccipital bone (Soc)], and the overlapping of the margins of several bones. This overlap or sliding over each other of these elements resembles old-fashioned telescopes.
Skull Anatomy
In some large terrestrial mammals, such as the elephant the skull is
vastly enlarged with pneumatized bones in part to accommodate the
large muscles of the head (Nickel et al., 1986). In contrast, the skulls
of the larger cetaceans (i.e., Ziphius and Eubalaena) are enlarged to
accommodate the larger muscle masses and larger food processing
requirements but are not pneumatized.
In diving mammals, air-filled cavities within rigid enclosures of
bone could be damaged during dives when subjected to large rapid
pressure changes associated with variations in depth. If air-filled
paranasal sinuses are present in divers, they have to be open-ended
so that air or other fluids (e.g., blood, lymph, cerebrospinal fluid) in
adjacent vascularized structures can move into and out of them to
compensate for changes in air volume in response to changes in ambient pressure (Molvaer, 2003); alternatively they must have flexible
walls that are capable of collapse. Of the carnivores, terrestrial bears
(Moore, 1981) have the most extensive sinuses; to our knowledge,
those of polar bears have not been described. Cetaceans particularly odontocetes, have several air-filled regions, those on the ventral
aspect of the skull are associated with pneumatized bones. These airfilled sinuses have large openings that are connected to the respiratory system via the Eustacean tube (Fraser and Purves, 1960; Houser
et al., 2004). Interestingly, in contrast to the pneumatized bones found
in terrestrial mammals, it is the cetacean pterygoid bones that are
the most pneumatized. Typically pterygoid bones are small in mammals but in cetaceans they are significantly enlarged (slightly more
than 40% of the ventral length of the skull in Ziphius; Rommel et al.,
2006). In many cetaceans, the pterygoid sinuses have thin medial and
lateral bony walls called lamellae. Some species with relatively large
pterygoid sinuses (e.g., ziphiids and physeterids) have lost the lateral
lamellae and the medial bony wall of the sinus is relatively thick (Fig.
13). In place of bony lateral lamellae, the large pterygoid sinuses of
these divers are walled with a tendinous sheath to which the muscles
of the palate attach (Fraser and Purves, 1960). In manatees, a large
ventromedial pterygoid process of the palatine bone and a large ventrolateral pterygoid process of the alisphenoid both join the relatively
small pterygoid bone to produce a robust structure that supports the
large pterygoid muscles (Figs 8, 10, and 12).
The walls of the pterygoid sinuses are well vascularized, perhaps
to help with adjusting volume as ambient pressures change. The airfilled spaces of live dolphins have been shown to be dynamic structures that function as reflectors to help isolate the earbones from the
sound producing apparatus of the head and to help isolate the two
ears so that they can have better directional abilities (Houser et al.,
2004).
VIII. Telescoping
Telescoping is a process often discussed when describing the skulls
of cetaceans (Figs 14, 15). The term, coined by Miller (1923), refers to
the elongation of the rostral elements and the dorsorostral movement
1045
of caudal elements (Kellogg, 1928; Miller, 1923; Rommel, 1990). The
relative placement of the skull bones in cetaceans results in considerable overlap of some adjacent bones. If the skull is sectioned, one can
observe as many as four different bones overlapping each other—this
overlap resembles old-fashioned collapsible telescopes. In cetaceans,
the external bony nares have been displaced to the dorsal apex of the
skull, so the nasal bones are located just caudal to the external bony
nares (as in other mammals) but dorsal to the brain case instead of at
the apex of the rostrum. The premaxillary and maxillary bones have
been extended at their rostral tips; their caudal aspects are pulled
up and back over the frontal bones and maintain their relative positions with the nasal bones. The narial passages are essentially vertical
in cetaceans, which eliminates the nasal bones as roofing bones of the
nasal passages. The nasal bones are, instead, relatively small vestiges
that lie in depressions of the frontal bones. Thus, the roof of the cetacean mouth is not the floor of the nasal passages as it is in most other
mammals. Caudally, telescoping differs in odontocete and mysticete
cetaceans (Fig. 14). The changes in the mysticetes are dominated by
a ventrocaudal extension of the maxillary bones, whereas in the odontocetes, the premaxillary and maxillary bones are shifted more dorsocaudally (Kellogg, 1928). Interestingly, whereas the odontocete facial
muscles have moved dorsocaudally over the eye, the temporal muscles
of the mysticetes have moved dorsorostrally over the eye. Thus, the
temporal fossae of the mysticetes are very different from those of the
odontocetes.
The remodeling associated with telescoping is reflected in the
number and positions of the cranial nerve foramina in the maxilla (Fig.
15). Consider the nerves that are associated with the muscles of the
face—the (sensory) trigeminal nerve (V) and the (motor) facial nerve
(VII). The right and left facial nerves control such muscle activity as
facial expression in the dog, feeding in the manatee, and focusing of
sonar pulses in the dolphin. The trigeminal nerves signal the brain to
coordinate the muscular activities in the same region. The relatively
large sizes of these two nerves in the dolphin and manatee reflect the
importance of these neuromuscular actions. The nerve diameters
are reflected by the size of the infraorbital foramina through which
the trigeminal nerve pierces the maxilla (Fig. 15). In odontocetes, the
bones and muscles of the face are reshaped and accommodate the
melon and its need for complex mechanical manipulation and the sensory and motor nerves are moved up and over the orbit. The homologous (and thus same-named) opening, which is infra-orbital in most
species, is now actually dorsal to the orbit (that is, supra-orbital) in
cetaceans!
In conclusion, we can state that a glance at a skull tells us a great
deal about an organism—how it senses its environment, how it feeds,
how big its brain is, etc. It is also very important in understanding
phylogenetic history and species description. Rather than becoming
bogged down in trying to memorize names of bones or bony features, study a skull with an open mind (pun intended) about adaptations and function.
Figure 14 (continued) One result of telescoping is the displacement of the external bony nares (and the associated nasal bones) toward
the dorsal apex of the skull—up and over the rostral margin of the brain! Telescoping is quite different in odontocete and mysticete cetaceans;
in most odontocetes the rostrum is dorsally concave, whereas in mysticetes the rostrum is ventrally concave. The temporal fossae of the mysticetes have moved up and forward over the eye; the temporal fossae in odontocetes are in a more typical mammalian position. Relatively more
bone mass is moved up and over the orbit in the odontocetes, whereas relatively more bone mass is moved down and under the orbit in mysticetes. In the lower schematic, arrows indicate the directions of relative movement as each skull is remodeled to accommodate the brain and
the respiratory, feeding, and acoustic apparatus of the two types of cetaceans. Note that in C the brains are scaled to fit in the lateral views
of the crania in B above them; the odontocete brain makes up a larger percentage of the cranial volume than does the brain of the mysticete.
Copyright S. A. Rommel.
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Skull Anatomy
V—trigeminal n.
VII—facial n.
Infraorbital
foramen
Nasal bones
Infraorbital
foramen (hidden)
'Infra'orbital
foramena
Maxillary bones
Figure 15 The nerves associated with the facial muscles also reflect telescoping. These are the trigeminal and the facial
nerves. Here the dog is compared with the manatee and the dolphin. The relatively large sizes of the trigeminal nerves are
reflected in the relatively large foramina through the maxillae (infraorbital foramina); the larger the nerve, the more information it can carry. The process of telescoping has remodeled the bones of the rostrum and included in this process are
the reshaping of the muscles of the face and the nerves that innervate them. Also note that some odontocete cetaceans have
notable bilateral asymmetry in the dorsal elements of the skull. Copyright S. A. Rommel.
See Also the Following Articles
Feeding Morphology ■ Sense Organs, Overview
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Sociobiology
FRITZ TRILLMICH
I. The Nature of Sociobiological Inquiry
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ociobiology is the study of social behavior and social evolution
based on the theory of adaptation through selection. As such it
is primarily concerned with the adaptiveness of social behavior
and the selective processes producing and maintaining adaptiveness.
Understanding the selective processes involved includes studying
the ecology, physiology, and behavior, as well as the demography and
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population genetics, of the species in question. Sociobiological investigation also increasingly attempts to characterize the genetic breeding
system, as well as the population dynamics and structure, which
importantly influence the effectiveness of evolutionary processes in
molding species characteristics.
The sociobiological approach assumes that selection at the individual level is the force producing adaptation. A proper understanding of social phenomena, therefore, needs an understanding of the
benefits and costs that the individual derives from its interaction
with the social environment. Explicitly, group selection is relegated
to a secondary position as in most circumstances selection operates
more strongly at the individual than at the group level because fertility, dispersal, and mortality events are more frequent and act much
more forceful on individuals than on groups. Explaining social phenomena such as group formation, parental care, and mating systems
from the action of selection at the level of the individual forms the
core of sociobiological inquiry.
As the majority of sociobiological research in the field of marine
mammals has been done on whales and pinnipeds, these two groups
form the focus of the following sections. Relevant information on sea
otters (Enhydra lutris) and manatees (Trichechus spp.) is mentioned
briefly in Section V.
II. Group Formation
The most obvious phenomenon of social life is group formation.
Suitable feeding or breeding habitat may initially lead to an aggregation of individuals, thus setting the stage for selective processes molding the evolution of elaborate social interactions. In contrast to the
term “aggregation,” “group” implies that individuals come together to
derive benefits from interactions that follow from this proximity. Such
a grouping may serve social, foraging, predator avoidance, or defense
against predators. Groups may also be established for mating and to
share parental care. These kinds of advantages constitute the selective
processes that promote group formation in a wide variety of animals.
Sociobiology tries to explain groupings from the advantages and disadvantages incurred by individuals (Krause and Ruxton, 2002).
A. Whales
The open ocean habitat offers few options for hiding from predators. Consequently, predation by large sharks and killer whales
(Orcinus orca), particularly on newborns, is one important factor
selecting for group formation in whales and dolphins. Direct observational evidence for this hypothesis is scarce, but signs of scarring
provide evidence of frequent encounters with predators. For example, about one-third of all humpback whale (Megaptera novaeangliae)
calves carry tooth marks on their flukes when arriving in the foraging
areas, presumably from encounters with killer whales or sharks during migration to the feeding grounds (Mann et al., 1999). The most
spectacular groupings are found in open ocean species such as spotted dolphins (Stenella spp.) which benefit most from the advantages
of grouping as protection against predators, but such species may also
benefit from group foraging.
Several effects play a role in the protection offered to an individual by a group. The “dilution effect” acts by reducing the probability of an individual to be attacked by a predator who has noticed
the group, if the predator takes only one individual out of the group.
This effect thus dilutes the chances of an attack on a given individual
dramatically (to 1/group size). The “confusion effect,” many individuals rushing back and forth through the visual field of an attacking
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