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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

To 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 informa-tion 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 mam-mals: the manatee ( Trichechus manatus ), the harbor seal ( Phocavitulina ), 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. Defi ning 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

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 fi rst three visceral arches, i.e., the lower jaw (or mandible) and the hyoid appa-ratus. 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 defi ned by the underlying bones ( Harper et al., 2008 ; Mead, 1975 ; Rommel et al ., 2006 ). The rela-tionships between the bones and the soft tissues of the head vary among species, perhaps with major differences in head and skull pro-fi les 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 infl uence the mechan-ics of locomotion, balance, and hearing. The completely aquatic spe-cies (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 specifi c characteristics of a skull (including dentition) often

refl ect the animal’s methods of feeding ( Figs 2, 3 ). For example, the “ typical ” heterodont dentition ( Kardong, 1998 ) of terrestrial car-nivores, such as the dog, is also found to various degrees in the seal, sea lion, sea otter, and polar bear. Heterodonty is tooth shape differ-ences 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 defi nitions are specifi c and are related to tooth attachment to the bones of the upper jaw ( Hildebrand, 1995 ). Incisors are found only in the premaxillary (inci-sive) bone; canines are found in the maxilla, in or very near the suture with the premaxilla. Incisors, canines, and premolars are decidu-ous teeth; molars are not. Developmentally, there are two sets—milk (or “ baby ” ) teeth and adult teeth. Premolars erupt from the maxil-lary 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 mak-ing 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

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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 (men-tal 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 fos-sil record) and specifi city of dentition contribute signifi cantly to our current understanding of the ecology and evolution of different taxa.

Harbor sealPhoca vitulina

California sea lion

Eubalaena glacialisNorthern right whaleBottlenose dolphin

Polar bear

Enhydra lutrisSea otter

Florida manateeTrichechus manatus latirostris

Ursus maritimus

Zalophus californianus

Tursiops truncatus

Domestic dogCanis familiaris

Figure 1 Skulls and fi rst 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.

Crushingmolars

Grindingcheek teeth

Shearingmolars

Shearingmolars

Shearingmolars

Dental formula: I 3/2, C1/1, P 3/3, M 1/2

Dental formula: I 3/3, C1/1, P 4/4, M 2/3

Dental formula: I 3/2, C1/1, P 4/4, M 1-2/1

Dental formula: I 3/2, C1/1, P 4/4, M 1/1

Dental formula: I 3/3, C1/1, P 2-4/2-4, M 2/3

All teeth similar20–26 per upper quadrant18–24 per lower quadrant

Shearingmolars

(Baleen extends fromupper jaw, medial and ventral to lower jaw)

Dental formula: I 0/0, C 0/0, Ck 5-8/5-8

DOGFOOD

Grasping and/or piercing teeth

Sieving plates of baleen

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.

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ing 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 mam-mals such as elephants and kangaroos. In addition, unusual for man-atees is the lifelong generation of new tooth buds, which develop in the dental capsule at the caudal end of each tooth row. Each mana-tee 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 ( Domningand 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 fl attened 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 fi sh, 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,

(A)

(B)

Tympanic

Tympanic bulla

(C)

Mandibularsymphysis

Coronoidprocess

Angle

Mandibular condyle

Mentalforamina

Angular process

Mandibular condyle

Coronoid process

Mandibular hiatus

Mandibular condyle

Angular process

Mandibularsymphysis

Mandibularsymphysis

Coronoid process

Mentalforamina

Mentalforamina

Mandibularforamen

Mandibular foramen

Body

Ramus

Body

Ramus

Body

Basihyal in two positions

Epihyal in two positions

Basihyal & thyrohyal

Stylohyal

Tympanic bulla

BasihyalEpihyal

Stylohyal

Ceratohyal

Thyrohyal

2

1

Dental capsule (with tooth buds)

Tympano & stylohyalcartilage

Tympanohyalcartilage

Epihyal &ceratohyalcartilage

Tympanohyalcartilage

Ceratohyal cartilage

TMJ

TMJ

TMJ

Thyrohyal cartilage

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 (posi-tion 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

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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 refl ected 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 fl esh without fi nely 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 chop-ping motion, using a simple hinge joint. Their temporomandibu-lar 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 refl ects feeding habits. In carnivores a dorsally-convex mandibular con-dyle of the dentary bone fi ts 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 mechani-cally constrained, allowing up and down movement but little or no transverse motion of the lower jaw. Of the skulls illustrated, the man-dibular fossa of the otter is the most restrictive with a deep concav-ity 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 con-strained because of their relatively large radii of curvature. Live dol-phins, however, exhibit simple up-and-down (opening-and-closing) jaw movements similar to those observed in the dog. As mentioned above, odontocetes have simple fi sh-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 fi brous

OccipitalMaxillaNasal Zygomatic arch

O – orbit, TF – temporal fossa, IF – infraorbital foramen, POF – postorbital process of the frontal, EAM - external acoustic meatus

External bony naris

Mandibular ‘fossa’

Occipital condyles(& foramen magnum)

EAM EAM

EAM

O TF

IF

O

TF

IF

POF

EAM

Nasal

OTF

IF

O

TF

IF

O TF

IF

O TF

IF

OTF

IF

O

IF

TF

POF POF

POF

POF

POF

POF

EAM

EAMEAM

EAM

Figure 4 Selected bony features of the cranium. The rostrum, composed of the premaxilla, maxilla, and occa-sionally the nasal, forms the “ face ” or muzzle of each species. The zygomatic arch, which supports the mas-seter 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 fl ow 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 mem-brane is visible in manatees but hidden within the middle ear of the other species. Copyright S. A. Rommel.

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structures that can absorb the mechanical shock associated with lunge feeding. Rorqual lower jaws must support the large, pleated gular sac into which fl ows 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 fl attened sub-cylinders that articulate with a distinct articular tuber-cle, which is located rostral to the shallow mandibular fossa ( Fig. 3 ). Manatees must have a relatively mobile TMJ to accommodate grind-ing their food. The motions of the manatee TMJ include infl uence 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 ros-tral 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 fl at 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 coor-dinated action of these muscles and bones as food leaves the oral cav-ity and moves through the pharynx. How do the bones of the head accommodate swallowing? The hyoid apparatus is an important struc-ture 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 suffi x - hyal to minimize confusion with hyoid mus-cles, Reidenberg and Laitman, 1994 ), provide the mechanical sup-port 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 confi guration 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 squid-eating beaked whales, pilot whales, and kogiids, the hyoid appara-tus 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 para-condylar (paroccipital) processes of the exoccipital bones (see below) in a position caudolateral to the tympanoperiotic complex. There are

distinct concavities for hyoid attachment in the paracondylar proc-esses ( 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 odon-tocetes (i.e., Kogia , Ziphius ) there are large, well-developed mastoid process of the tympanoperiotic. These mastoid processes are simi-lar 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 caudola-teral 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 special-

ized bony features ( Fig. 4 ). Bony features are morphological charac-ters or landmarks that make up one or more bones. Size, shape, and positions of bony features refl ect 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; zygo-matic 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 cau-dally (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 project-ing 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 refl ect respiratory adaptations to diving, feeding, and locomotion. The occipital condyles position the head on the neck and infl uence the fl exibility 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 fi rst 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 ossifi cation centers in a basic pattern that par-tially or completely encloses the brain and encapsulates the sensory

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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 homolo-gous between species? A systematic but simplifi ed approach that allows one to compare homologous elements is to utilize a general-ized 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 ).

Nasal cavity

Oral cavity

Esophagus

Trachea

Palate

Air

FoodEpiglottis positions

Air

Food

Blowhole

Naris

Cranial cavity

Cranial cavity

Melon

Diverticulum

Soft palate

Tongue

Hard palate

EpiglottisTrachea

Nasal bone

C7

Atlas-axis, C1-C2

C7

C6

Tongue

Epiglottis Trachea

Axis, C2

Hard palate

Soft palate

Naris

Cranial cavity

Esophagus

TracheaOral cavity

Nasal bone

Air

Food

Food

Air

Cut bone, hard palate

Soft palateEpiglottal cartilage, nasal bone

Frontal sinus

Soft palate

TongueEpiglottis (goose beak)Hard palate

Bony nasal passage (choana)Nasal bone

Axis, C2

Choana

Choana

Rim of choana

Rim of choana

Rim of choana

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 modifi ed accordingly. The dog and manatee are schematically represented in the upper panel. In the dolphin (lower panel) further modifi cation is shown to accommodate the migration of the respiratory opening to the top of the head. Copyright S. A. Rommel.

Spinal cord

n. II

n. VIII

Olfactory capsule

Optic capsule

Brain “capsule”

Orbitosphenoid

Presphenoid

Exoccipital

Ossification centers

Basisphenoid

Otic (peri-otic)

Ethmoid

n. IOlfactory sac

Lens

Olfactory lobe

Retina

Otocyst

Prechordal cartilage

Parachordal cartilage

Otic capsule

(Cartilagenousneurocranium)

Basioccipital

Cartilage

Nerve tissue

earlier in development cartilaginous neurocraniumlater in developmentCartilaginous neurocranium Ossification centers in theCartilaginous neurocranium

Figure 6 Schematic illustration of ventral views of the developing vertebrate skull. Modifi ed 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 ossifi ca-tion centers that will eventually become the replacement bones of the cranium .

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1 We have used three different terms incorporating the word “ bone ” . Bones are discrete ossifi cations 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).

Tympanic, Tym

Supraoccipital, Soc*

Squamosal, Sqa

Premaxilla, Pmx

Periotic, Per*

Parietal, Par

Orbitosphenoid, Osp*

Nasal, Nas

Maxilla, Max

Lacrimal, Lac

Interparietal, Int

Frontal, Frn

Exoccipital, Exo*

Ethmoturbinate, eTur

Cribriform plate, Crb*

Basisphenoid, Bsp*

Basioccipital, Boc*

Alisphenoid, Als*

Ethmoid, Eth*

Vomer, Vom

Presphenoid, Psp*

Palatine, PalPterygoid, Pty

Jugal, Jug

Dentary, Den

Thryohyal, tHyo*Maxilloturbinate, mTur

Nasoturbinate, nTur

Ceratohyal, cHyo*

Epihyal, eHyo*

Stylohyal, sHyo*

Tympanohyal, tHyo*

Basihyal, bHyo*

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 frame-work in which to compare a wide variety of mammalian skulls. Modifi ed 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 com-pound bones 1 ; 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 ossifi cation centers ( Kentand Miller, 1997 ). These separate bones include the squamosal, the periotic, the tympanic, the middle ear ossicles, and in some spe-cies 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 terres-trial 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 fi t 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 basi-occipital, 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.

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 con-nective tissue). Joints between adjacent cranial bones are referred to as sutures or synchondroses. Sutures are fi brous joints between der-mal bones; synchondroses are cartilaginous joints between endochon-dral 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 fl exibility for a relatively large brain within the cra-nium to pass through a relatively narrow birth canal. In the illustration of the exploded manatee cranium ( Fig. 8 ), the hatched regions repre-sent ( 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 refl ects 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 dif-ferent parts of the same joint, probably to refl ect 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 confi gurations 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 system-atic 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

Skull Anatomy1040

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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

refl ected 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

Frontal, Frn

Supraoccipital, Soc

Exoccipital, Exo

Premaxilla, Pmx

Squamosal, Sqa

Orbitosphenoid, Osp

Lacrimal, Lac

Basioccipital, Boc

Basisphenoid, Bsp

Alisphenoid, Als

Jugal, Jug

Maxilla, Max

Parietal, Par

Tympanic, Tym

Periotic, Per

Malleus, Mal

Palatine, Pal

Nasal, Nas

Overlapping sutures

Pterygoid, Pty

Rommel 08

Figure 8 Left lateral view of an exploded cranium of the Florida manatee. This fi gure illustrates the overlap-ping and/or abutting margins of bones that make up the sutures and synchondroses of the cranium. Copyright S. A. Rommel.

Pmx

Max Jug

Nas

Frn

PtyPal Tym

Par

Exo*

Boc*

Pal

Als*

Lac Soc*

Osp*

Sqa

Pmx

Max

Nas

JugFrn

Pal Pty

ParLac

Soc*

TymSqa

Frn Osp*Nas

Als*

Exo*

Max Jug

Soc*Pmx

Tym

SqaPar

PalPty

Lac*

Boc*

Osp*

TymSqaPal Pty

ParFrn

Max

Nas

Pmx

Exo*

Soc*

Vom

Osp*

PmxMax

Par

Sqa

Frn

Jug

Lac

SqaTym

Boc*Exo*

Soc*Nas Frn

Pal

Pmx

Max JugPal

Pmx

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Lac

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Sqa

ParSoc*

FrnNas

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Boc*Exo*

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JugFrn

PalPty

ParLac

Soc*

Tym

Sqa

Boc*

Exo*

Als*

Jug

Exo*Sqa

Bsp Boc*Tym

Per*

Max Pal

Max

Pmx

Als*

Par Soc*Lac

Jug

Frn Osp*

Pty

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 modifi ed in each species. Endochondral bones are indicated with an asterisk. Copyright S. A. Rommel.

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nerve or blood vessel may be completely surrounded by a bone or bones of the skull, resulting in a specifi c foramen. Because this proc-ess 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 dif-ferent ages, instead of a single foramen for each individual nerve, one or more nerves may exit the braincase through a single open-ing. 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 open-ings: optic foramen, orbital fi ssure (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 fi rmly 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 isola-tion from the rest of the skull; in cleaned skulls the earbone com-plexes 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 fi ssure, which is an irregu-lar 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 ter-restrial mammals, the margins of the petrooccipital fi ssure 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 alveo-lar vessels and nerves. In manatees, the mandibular foramen is rela-tively 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 fi lled 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 audi-tory meatus is a long narrow canal ( Fig. 13 ) ( Rommel et al ., 2006 ). Interestingly, as mentioned above, these cetaceans have distinct mas-toid bones. Fraser and Purves (1960) describe secondary growth of the basioccipital, parietal, and squamosal bones around the margins

(B) (C)(A)

Cartilage

SQA

SER

FOLSER

SER

PLA

PLASQA

SYN

SYN

FOL

PLA SQA SYNSERFOL

SQA

cut bones

PLASQA

SYN

SYN

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SYN

SER

SYN

SER

FOL

SER

SERPLA

SQA

SQAPLA SER

SQA

PLA

FOL

PLA

FOLFOL

FOL

Figure 10 Joint types in the cranium of the dog (A), manatee (B), and dolphin (C). Sutures are fi brous joints between dermal bones; synchondroses are cartilaginous joints between endochondral bones. Joints allow growth of adjacent bones, provide limited fl exibility and absorb mechanical forces. Suture types are defi ned 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 overlap-ping 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, simplifi ed, sagittally sectioned crania illustrate those joints that can be observed on the midline. Defi nitions are from a variety of sources; parenthetical names are from Schaller (1992) . Copyright S. A. Rommel.

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of the cranial hiatus, which narrows and elongates the channels for the facial and acoustic nerves.

VII. Skull Cavities The cranial cavity ( Figs 5 and 13 ) houses the brain, its menin-

ges, 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 fl oor 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 orbit-osphenoid 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 diffi cult to recog-nize 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 pro-longed 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 ceta-ceans. 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 sep-tum 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 basi-sphenoid and presphenoid bones ( Fig. 12 ).

Conchae (turbinates, turbinals) are thin lamellae of bone (cov-ered with mucous membrane in life) that project into the nasal cav-ity. 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 telescop-ing below) and are devoid of conchae; the bones dividing and bor-dering 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 fi lling the nasal cavity with lace-like networks of bone. These structures signifi -cantly 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 rela-tively recently in engineering history has man built composite struc-tures (monocoques) that approach the effi ciency 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-fi lled 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

Vmn

III,IV

Vmx

V ,VIo

IX,X,XI

VII

XII

Orbit

Nasalcapsule

Braincase

Earcapsule

Cribriformplate

Opticforamen

Orbitalfissure

Foramenrotundum

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Jugularforamen

Hypoglossalforamen

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II

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 cri-briform plate, found at the rostral margin of the braincase, is associ-ated 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 fi ssure is usually at the orbitosphenoid bone-alisphenoid bone suture (also anterior lacerate foramen; III-ocu-lomotor 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 stylomas-toid 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 mea-tus.) 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 perfo-rates 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.

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Sless weight than other bony structures. In the skull bones of most placental mammals, pneumatized paranasal sinuses develop embry-onically 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 head 2 . Some paranasal

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 ; Nickelet 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 ).

Pmx Vestigial alveolus

Pterygoid proc., Pal

Pmx

Vom

Jug

Pal

Max

Boc crest

Antorbital notch

Major palatine for.

Jugular notch

(C)

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BocExo

Sqa

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Par

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Vom

Paracondylar proc., Exo

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Vent. infraorbital for.

Orbital fis. (II-VI)

Foramen ovale (V3)

Supraorbital proc., Frn

Pty crest

Rim of L choana

Cranial hiatus (IX-XI)

for. magnum

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Occipital condylefor. magnum

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Rim of L choanaOrbital fis. (II-VI)

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for. magnum

Bsp

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Pterygoid proc., Pty

Lamalle of Pty sinus

Postglenoid proc.Postglenoid proc.Pty

Hypoglossal for. (inconstant)

Postorbital proc., Frn

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Max Major palatine for.

Optic for. (II)Orbital fis. (III-VI)

for. ovale (V3)Stylomastoid for. (VII)

Jugular for. (IX-XI)Hypoglossal for. (XII)

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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 fi rmly 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; fi s, fi ssure; 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.

2 Similar bracing systems are found in the wings and fuselages of aircraft and the hulls of large ships ( Gordon 1988 ).

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Long narrow channels for cranial nerves

VII & VIII

(A)

(B)

Cranialhiatus

Squamosal

Tympanoperiotic

Basioccipitalcrest

Cranial cavity Parietal

Supraoccipital

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. Modifi ed from Rommel et al. (2006) .

OrbitBrain

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Max onlyBrain

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NasalsNasals

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Temporalfossa

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Externalnares

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(A)

(B)

(C)

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 dorso-rostral movement of the caudal elements [particularly the supraoccipital bone (Soc)], and the overlapping of the mar-gins of several bones. This overlap or sliding over each other of these elements resembles old-fashioned telescopes.

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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-fi lled 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-fi lled paranasal sinuses are present in divers, they have to be open-ended so that air or other fl uids (e.g., blood, lymph, cerebrospinal fl uid) in adjacent vascularized structures can move into and out of them to compensate for changes in air volume in response to changes in ambi-ent pressure ( Molvaer, 2003 ); alternatively they must have fl exible 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 particu-larly odontocetes, have several air-fi lled regions, those on the ventral aspect of the skull are associated with pneumatized bones. These air-fi lled sinuses have large openings that are connected to the respira-tory 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 mam-mals but in cetaceans they are signifi cantly 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 ven-trolateral 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 air-fi lled spaces of live dolphins have been shown to be dynamic struc-tures that function as refl ectors 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

of caudal elements ( Kellogg, 1928 ; Miller, 1923 ; Rommel, 1990 ). The relative placement of the skull bones in cetaceans results in consider-able 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 posi-tions with the nasal bones. The narial passages are essentially vertical in cetaceans, which eliminates the nasal bones as roofi ng 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 ceta-cean mouth is not the fl oor 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 odon-tocetes, the premaxillary and maxillary bones are shifted more dorso-caudally ( 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 refl ected 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 refl ect the importance of these neuromuscular actions. The nerve diameters are refl ected 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 sen-sory and motor nerves are moved up and over the orbit. The homolo-gous (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 fea-tures, study a skull with an open mind (pun intended) about adapta-tions 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 mysti-cetes 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 mys-ticetes. 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 fi t 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.

Skull Anatomy1046

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See Also the Following Articles Feeding Morphology ■ Sense Organs, Overview

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Harper, C. J., McLellan, W. A., Rommel, S. A., Gay, D. M., Dillaman, R. M. and Pabst, D. A. (in press, 2008) Morphology of the melon and its tendinous connections to the facial muscles in bottlenose dolphins (Tursiops truncatus ). J. Morphol .

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VII—facial n.

V—trigeminal n.

Nasal bones

Maxillary bones

'Infra'orbitalforamena

Infraorbitalforamen

Infraorbitalforamen (hidden)

Figure 15 The nerves associated with the facial muscles also refl ect 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 refl ected in the relatively large foramina through the maxillae (infraorbital foramina); the larger the nerve, the more infor-mation 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.

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Sociobiology FRITZ TRILLMICH

I. The Nature of Sociobiological Inquiry

Sociobiology 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

population genetics, of the species in question. Sociobiological investi-gation also increasingly attempts to characterize the genetic breeding system, as well as the population dynamics and structure, which importantly infl uence the effectiveness of evolutionary processes in molding species characteristics.

The sociobiological approach assumes that selection at the indi-vidual level is the force producing adaptation. A proper understand-ing of social phenomena, therefore, needs an understanding of the benefi ts 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 fertil-ity, dispersal, and mortality events are more frequent and act much more forceful on individuals than on groups. Explaining social phe-nomena 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 fi eld 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 briefl y 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 aggrega-tion of individuals, thus setting the stage for selective processes mold-ing the evolution of elaborate social interactions. In contrast to the term “ aggregation, ” “ group ” implies that individuals come together to derive benefi ts 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 disad-vantages incurred by individuals ( Krause and Ruxton, 2002 ).

A. Whales The open ocean habitat offers few options for hiding from pred-

ators. 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 obser-vational evidence for this hypothesis is scarce, but signs of scarring provide evidence of frequent encounters with predators. For exam-ple, about one-third of all humpback whale ( Megaptera novaeangliae)calves carry tooth marks on their fl ukes when arriving in the foraging areas, presumably from encounters with killer whales or sharks dur-ing migration to the feeding grounds ( Mann et al. , 1999 ). The most spectacular groupings are found in open ocean species such as spot-ted dolphins ( Stenella spp.) which benefi t most from the advantages of grouping as protection against predators, but such species may also benefi t from group foraging.

Several effects play a role in the protection offered to an indi-vidual by a group. The “ dilution effect ” acts by reducing the prob-ability 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 individ-uals rushing back and forth through the visual fi eld of an attacking