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Skeleton, Postcranial 1021 S V. Growth and Development Florida manatee calves average about 120 cm in length at birth, but viable calves may have a birth length ranging from about 80 to 160 cm. This, along with variable individual growth rates, results in a highly variable length at age distribution. For example, 2-year-old manatees at Blue Spring (Florida) may range from 210 to 260 cm total length. From a sample of carcasses of Florida manatees in the age class 1 and 2 years, total lengths ranged from about 120 to over 260 cm. Florida manatees grow rapidly during the first few years, and body length becomes asymptotic at about 300 cm and an age of 8-10 years. The birth weight for Florida manatees ranges from 30 to 50 kg and the average adult body weight is about 500 kg. The Antillean and West African manatees are probably similar to the Florida manatee in these respects. The Amazonian manatee is smaller and has a birth length of 85–100 cm and a birth weight of 10–15 kg. Large adults may reach lengths of 280 cm and weights of 480 kg. The dugong has a birth length of 100–130 cm and a birth weight of 25–35 kg. Adult dugongs average 270 cm in length and 250–300 kg body weight. VI. Fecundity As with other aspects of sirenian life history, data on fecundity are limited and based primarily on studies of the Florida manatee and the dugong. A key factor in assessing fecundity is the gestation period, which, despite numerous conceptions and births of Florida mana- tees, is not known for any sirenian species. However, scientists gen- erally agree that gestation for the Florida manatee and the dugong is in the range of 12–14 months and that the other species of sirenians are probably similar. The known inter-birth interval for wild Florida manatees averages 2.5–2.6 years. The estimated inter-birth interval for Florida manatees ranges from 2.5 to 3.0 years when gestation period estimates of 12, 13, and 14 months are applied. This suggests that the true gestation period may be close to 12 months. Estimated inter-birth intervals for the dugong range from 2.7 to 5.8 years depending on the length of the gestation period assumed (12, 13, or 14 months) and the population of dugongs used. We do know that Florida manatees resume estrous cycling within 1–2 months after the loss of a calf and become pregnant shortly thereafter. Whereas manatees and dugongs (both males and females) display seasonal reproductive activity, there is scant evidence to suggest that they have reproductive senescence as many mammals, including humans, do. Other factors important in the calculation of fecundity are the number of offspring per birth and the sex ratio of offspring at birth. Wild Florida manatees have been documented producing twin off- spring (but no more) in about 1.4–1.8% of births. Estimates of twinning based on Florida manatee carcass studies are as high as 4%. Limited and/or anecdotal data suggest that twinning occurs in the Antillean manatee and in the dugong. The sex ratio of the offspring at birth appears to be 1:1 for both the Florida manatee and the dugong. It is probably reasonable to assume that both Amazonian and West African manatees have similar patterns of twinning and offspring sex ratio. Applying all of our knowledge of and assumptions about Florida manatee life history, the average fecundity (number of female births per female per year) for age classes 4–29 years was estimated at 0.189, 0.238, and 0.127 using different sets of data obtained from the exam- ination of carcasses. Similarly, estimates of annual pregnancy rate (APR) and gross annual recruitment rate (GARR) ranged from 0.190 to 0.394 and 0.044 to 0.90, respectively, depending on the set of car- cass data and gestation period used. Similar calculations for the dug- ong based on a smaller data set yielded apparent (annual) pregnancy rates of 0.093–0.353 over a series of years. Both the State of Florida (Haubold et al., 2006; Florida Fish and Wildlife Conservation Commission, 2006) and the US Fish and Wildlife Service (2007) have used life history parameters to assess the status of the Florida manatee. These reports include references to several population modeling projects that were in progress and that were not (at the time the reports were released) available for general public con- sumption in the peer-reviewed or gray literature. VII. Summary Even though the Florida manatee and the dugong have been studied intensively since the 1980s, detailed data on many aspects of their life history are only beginning to be elucidated and there is considerably less information on the other species of sirenians. Given the threatened or endangered status of this unique group of marine mammals, every effort should be made to learn about their biology so that we may ensure their survival. DKO has been involved with marine mammal studies since 1965 and has worked on pinnipeds, Sirenians and the smaller cetaceans. He has held positions at the University of Miami’s Rosenstiel School of Marine and Atmospheric Science, and in Corporate Zoological Operations for the Busch Entertainment Corporation (SeaWorld and Bush Gardens parks). He has served as president of the Society for Marine Mammalogy and president of the Florida Academy of Sciences. He has worked on sirenians, particularly the Florida manatee, since 1974 and was a co-founder of the Florida manatee carcass salvage program. See Also the Following Articles Dugong Manatees References Florida Fish and Wildlife Conservation Commission (2006). “Draft man- atee management plan Trichechus manatus latirostris.” Florida Fish and Wildlife Conservation Commission, Tallahassee, FL 32399, USA. Hartman, D. S. (1979). “Ecology and Behavior of the Manatee (Trichechus manatus) in Florida.” American Society of Mammalogists, Special Publication No. 5. Lawrence, Kansas, USA. Haubold, E. M., Deutsch, C., and Fonnesbeck, C. (2006). “Final biologi- cal status review of the Florida manatee ( Trichechus manatus latiros- tris).” Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, St. Petersburg, FL. O’Shea, T. J., Ackerman, B. B., and Percival, H. F. (eds.) (1995). “Population Biology of the Florida Manatee.” Information and Technology Report 1. U.S. Department of the Interior, National Biological Service, Washington, DC. Reynolds, J. E., III, and Odell, D. K. (1990). “Manatees and Dugongs.” Facts on File, New York. Reynolds, J. E., III, and Rommel, S. A. (eds) (1999). “Biology of Marine Mammals.” Smithsonian Institution Press, Washington, D.C. Ricklefs, R. E. (1973). “Ecology .” Chiron Press, Portland, OR. Ridgway, S. H., and Harrison, R. J. (eds) (1985). “Handbook of Marine Mammals,” Vol. 3. Academic Press, London. Skeleton, Postcranial SENTIEL ROMMEL AND JOHN E. REYNOLDS, III T he postcranial skeleton includes all the bones and cartilages caudal to the head skeleton; it is subdivided into axial com- ponents (the vertebral column, ribs, and sternebrae, which

Transcript of Skeleton, Postcranial - University of California, San Diegocetus.ucsd.edu/SIO133/PDF/Skeleton...

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V. Growth and Development Florida manatee calves average about 120 cm in length at birth, but

viable calves may have a birth length ranging from about 80 to 160 cm. This, along with variable individual growth rates, results in a highly variable length at age distribution. For example, 2-year-old manatees at Blue Spring (Florida) may range from 210 to 260 cm total length. From a sample of carcasses of Florida manatees in the age class � 1 and � 2 years, total lengths ranged from about 120 to over 260 cm.Florida manatees grow rapidly during the fi rst few years, and body length becomes asymptotic at about 300 cm and an age of 8-10 years. The birth weight for Florida manatees ranges from 30 to 50 kg and the average adult body weight is about 500 kg. The Antillean and West African manatees are probably similar to the Florida manatee in these respects. The Amazonian manatee is smaller and has a birth length of 85–100 cm and a birth weight of 10–15 kg. Large adults may reach lengths of 280 cm and weights of 480 kg. The dugong has a birth length of 100–130 cm and a birth weight of 25–35 kg. Adult dugongs average 270 cm in length and 250–300 kg body weight.

VI. Fecundity As with other aspects of sirenian life history, data on fecundity are

limited and based primarily on studies of the Florida manatee and the dugong. A key factor in assessing fecundity is the gestation period, which, despite numerous conceptions and births of Florida mana-tees, is not known for any sirenian species. However, scientists gen-erally agree that gestation for the Florida manatee and the dugong is in the range of 12–14 months and that the other species of sirenians are probably similar. The known inter-birth interval for wild Florida manatees averages 2.5–2.6 years. The estimated inter-birth interval for Florida manatees ranges from 2.5 to 3.0 years when gestation period estimates of 12, 13, and 14 months are applied. This suggests that the true gestation period may be close to 12 months. Estimated inter-birth intervals for the dugong range from 2.7 to 5.8 years depending on the length of the gestation period assumed (12, 13, or 14 months) and the population of dugongs used. We do know that Florida manatees resume estrous cycling within 1–2 months after the loss of a calf and become pregnant shortly thereafter. Whereas manatees and dugongs (both males and females) display seasonal reproductive activity, there is scant evidence to suggest that they have reproductive senescence as many mammals, including humans, do.

Other factors important in the calculation of fecundity are the number of offspring per birth and the sex ratio of offspring at birth. Wild Florida manatees have been documented producing twin off-spring (but no more) in about 1.4–1.8% of births. Estimates of twinning based on Florida manatee carcass studies are as high as 4%. Limited and/or anecdotal data suggest that twinning occurs in the Antillean manatee and in the dugong. The sex ratio of the offspring at birth appears to be 1:1 for both the Florida manatee and the dugong. It is probably reasonable to assume that both Amazonian and West African manatees have similar patterns of twinning and offspring sex ratio.

Applying all of our knowledge of and assumptions about Florida manatee life history, the average fecundity (number of female births per female per year) for age classes 4–29 years was estimated at 0.189, 0.238, and 0.127 using different sets of data obtained from the exam-ination of carcasses. Similarly, estimates of annual pregnancy rate (APR) and gross annual recruitment rate (GARR) ranged from 0.190 to 0.394 and 0.044 to 0.90, respectively, depending on the set of car-cass data and gestation period used. Similar calculations for the dug-ong based on a smaller data set yielded apparent (annual) pregnancy rates of 0.093–0.353 over a series of years. Both the State of Florida

( Haubold et al., 2006 ; Florida Fish and Wildlife Conservation Commission, 2006 ) and the US Fish and Wildlife Service (2007) have used life history parameters to assess the status of the Florida manatee. These reports include references to several population modeling projects that were in progress and that were not (at the time the reports were released) available for general public con-sumption in the peer-reviewed or gray literature.

VII. Summary Even though the Florida manatee and the dugong have been

studied intensively since the 1980s, detailed data on many aspects of their life history are only beginning to be elucidated and there is considerably less information on the other species of sirenians. Given the threatened or endangered status of this unique group of marine mammals, every effort should be made to learn about their biology so that we may ensure their survival.

DKO has been involved with marine mammal studies since 1965 and has worked on pinnipeds, Sirenians and the smaller cetaceans. He has held positions at the University of Miami’s Rosenstiel School of Marine and Atmospheric Science, and in Corporate Zoological Operations for the Busch Entertainment Corporation (SeaWorld and Bush Gardens parks). He has served as president of the Society for Marine Mammalogy and president of the Florida Academy of Sciences. He has worked on sirenians, particularly the Florida manatee, since 1974 and was a co-founder of the Florida manatee carcass salvage program.

See Also the Following Articles Dugong ■ Manatees

References Florida Fish and Wildlife Conservation Commission ( 2006 ). “ Draft man-

atee management plan Trichechus manatus latirostris . ” Florida Fish and Wildlife Conservation Commission , Tallahassee, FL 32399, USA .

Hartman , D. S. ( 1979 ). “ Ecology and Behavior of the Manatee (Trichechus manatus ) in Florida . ” American Society of Mammalogists , Special Publication No. 5 . Lawrence, Kansas, USA.

Haubold , E. M. , Deutsch , C. , and Fonnesbeck , C. ( 2006 ). “ Final biologi-cal status review of the Florida manatee ( Trichechus manatus latiros-tris ) . ” Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute , St. Petersburg, FL .

O’Shea, T. J., Ackerman, B. B., and Percival, H. F. (eds.) (1995). “ Population Biology of the Florida Manatee. ” Information and Technology Report 1. U.S. Department of the Interior, National Biological Service, Washington, DC.

Reynolds , J. E. , III , and Odell , D. K. ( 1990 ). “ Manatees and Dugongs . ” Facts on File , New York .

Reynolds , J. E. , III , and Rommel , S. A. (eds) ( 1999 ). “ Biology of Marine Mammals . ” Smithsonian Institution Press , Washington, D.C .

Ricklefs , R. E. ( 1973 ). “ Ecology . ” Chiron Press , Portland, OR . Ridgway , S. H. , and Harrison , R. J. (eds) ( 1985 ). “ Handbook of Marine

Mammals , ” Vol. 3 . Academic Press , London .

Skeleton, Postcranial SENTIEL ROMMEL AND JOHN E. REYNOLDS , III

The postcranial skeleton includes all the bones and cartilages caudal to the head skeleton; it is subdivided into axial com-ponents (the vertebral column, ribs, and sternebrae, which

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are “ on ” the midline) and appendicular components (the forelimbs, hindlimbs, and pectoral and pelvic girdles, which are “ off ” the mid-line). The skeleton supports and protects soft tissues, controls modes of locomotion, and predominantly determines overall body size and shape. The marrow of some bones may generate the precursors to certain blood cells. Skeletal elements may store lipids (particularly in the Cetacea) and calcium (particularly in the Sirenia) and thus infl u-ence buoyancy ( Kipps et al. , 2002 ). Because bones are continuously remodeled in response to biochemical and biomechanical demands over the life span of the marine mammal, they offer information that can help interpret life history events after death.

We discuss the skeletons of seven different species of marine mammals: the Florida manatee ( Trichechus manatus latirostris ), the harbor seal ( Phoca vitulina ), the California sea lion ( Zalophuscalifornianus ), the North Atlantic right whale ( Eubalaena glacialis ), the bottlenose dolphin ( Tursiops truncatus ), the polar bear ( Ursusmaritimus ), and the sea otter ( Enhydra lutris ). We use the domes-tic dog skeleton ( Canis familiaris ) to provide a familiar reference. These marine mammal species were chosen, in part, because much is known about them and they provide a wide range of biomechani-cal morphologies. The skull morphology of these seven species is described in the chapter entitled skull anatomy of this encyclope-dia. The manatee, dolphin, and right whale represent the many spe-cies that have lost their hindlimbs and are permanently aquatic; the other species may spend at least some of their life on land.

Visualize the articulated (assembled) skeleton by fi rst consider-ing individuals in an absolute sense (left and lower parts of Fig. 1 ) and then in a relative sense (upper right of Fig. 1 ). Consider what decisions morphologists make when comparing features among indi-viduals that differ substantially in size. Contrast the two methods of scaling by using the human swimmer as a reference. Because rela-tional comparisons (such as proportions and percentages) are intui-tive, we use the relative scheme for most of this chapter.

We will refer to the manatee when describing individual morpho-logical structures but refer to the seven selected marine mammal species when discussing marine mammals in general (for details on the same structures in the dolphin, see Rommel 1990 ; for the true seals, see Pierard, 1971 ; Pierard and Bisaillon, 1978 ; for the dog, see Evans, 1993 ; for mammals in general, see Flower, 1885 ).

I. Axial Skeleton A. Vertebral Structures

A few terms are necessary to better grasp the functional mor-phology of the vertebral column. Each vertebra (plural vertebrae) has several parts ( Fig. 2A ). The body or centrum (plural-centra) of each vertebra forms the primary mechanical support of the verte-bral (spinal) column ( Fig. 2B ). Several projecting parts or processesmay extend from the centrum and provide connective tissue attach-ment sites, protection for soft tissues, or both. The largest and most common lateral processes are transverse processes, which tend to be long and robust in the lumbar vertebrae. In the cervical region, there may be two transverse processes extending from each side of a single vertebra.

Dorsal to the centrum is the neural arch, an arch of bone that protects the spinal cord. Interestingly, in some marine mammal spe-cies, the neural arch is considerably enlarged to accommodate rel-atively large masses of vascular tissue and/or fat that surround the spinal cord. Because of these enlargements, the neural canal may not refl ect the dimensions of the spinal cord as it does in most terres-trial species ( Giffen 1992 ). In addition, each neural arch may extend

dorsally as a neural spine (spinous process). Neural spines function as levers to increase the mechanical advantage of the epaxial (epi-axial) muscles to dorsofl ex the body ( Pabst, 1993 ).

Relative motion between adjacent vertebrae is controlled, in part, by the size and shape of the intervertebral disks ( Fig. 2C ). Intervertebral disks are fl exible yet resist compression; they consist of a fi brous outer ring, the annulus fi brosus and a gelatinous inner mass, the nucleus pulposis . The jelly-like nucleus forms a dynamic joint that can adjust its shape within the elastic fi bers of the annu-lus. Intervertebral disks are resilient structures that support complex forces of bending. The same design of surrounding a deformable core with elastic fi bers is used in baseballs and golf balls.

Flexibility of the vertebral column depends, in part, on the thick-ness of the disks. Disk thickness varies within and among species, and intervertebral disks represent a substantial proportion (10–30%) of the length of the vertebral column. Relaxed (neutral) curvature of the vertebral column is determined by the shapes of the indi-vidual vertebrae, not by the shapes of the intervertebral spaces. Intervertebral disks provide fl exibility, whereas curvature is provided by (nonparallel) vertebral body faces ( Fig. 3 ).

Adjacent vertebrae may have other surfaces of articulation (fac-ets); zygapophyses (singular, zygapophysis) may be located on the neural arch, neural spine, and/or the transverse processes. Zygapophyses are bilaterally paired articular facets, found on the cra-nial and caudal aspects of each vertebra ( Fig. 2D ). The cranial pair are termed prezygapophyses , and the caudal pair postzygapophyses . The region of articulation between prezygapophyses and postzyga-pophyses is typically a synovial joint if the facets overlap.

The zygapophyses in the neck and cranial thorax tend to be ori-ented horizontally to allow axial rotation (twisting) and lateral (side-to-side) motions. The zygapophyses in the caudal thorax and tail tend to be oriented vertically to facilitate dorsoventral (up-and-down) motions. In some regions of the vertebral column adjacent vertebrae may have reduced or absent zygapophyses. Test these zygapophyseal constraints on yourself by bending and twisting your body—note how your thorax (rib-bearing region) fl exes (most of the axial rota-tion and some lateral fl exion occurs here) when compared with your lumbar (low back) region (where most of the allowable dorsoventral fl exion occurs).

B. Vertebral column Traditionally, the typical mammalian vertebral column is sepa-

rated into fi ve regions, each of which is defi ned by what is or is not attached to the vertebrae. These regions are cervical, thoracic ( “ dorsal ” in the older literature), lumbar, sacral, and caudal ( Fig. 3 ).The vertebral formula is an alpha-numerical abbreviation for the numbers of vertebrae in each region. For example C6:T17:L1:S0:Ca25 describes the 6 cervical, 17 thoracic, 1 lumbar, 0 sacral, and 25 caudal vertebrae in the Florida manatee. Individual vertebrae in each region are also referred to by their position using one or two (regiospecifi c) letters and a number. For example, the third cervical vertebra is designated as C3. The total number of vertebrae, exclud-ing the caudal vertebrae, is surprisingly close to 30 in most mammals ( Flower and Lydekker 1891 ). Using the vertebral formula, contrast the vertebral column of the selected species ( Fig. 3 ).

C. Cervical Region Cervical vertebrae ( Figs. 3, 4A ) are cranial to the rib-bearing ver-

tebrae of the thorax. Most mammals have seven cervical vertebrae; but all the sirenians and the two-toed sloth ( Choloepus) have six and

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2.2–3.0 m

1.5–1.8 m

1.3–1.5 m

3.5–4.1 m

1.5–3.5 m

Reference distanceshoulder to hip

Harbor seal

California sea lion

Bottlenose dolphin

Polar bear

Sea otter

Florida manatee

Domestic dog

Reference line 1 m

1.5–2 m

Florida manatee

Sea otter

California sea lion

Harbor seal

Bottlenose dolphin

Domestic dog

1.8–2.5 m

Polar bear

13–16 m

North Atlantic right whaleNorth Atlantic right whale

Figure 1 Selected marine mammal skeletons (the Florida manatee, the harbor seal, the California sea lion, the North Atlantic right whale, the bottlenose dolphin, the polar bear, and the sea otter) compared with the skeleton of the domestic dog. The drawings on the left and bottom are scaled so that 1 m on any one species equals 1 m on all the others in this group. The range of adult total body lengths (snout-tip to tail-tip; note that human height is measured differently) is given in meters beneath each drawing. This group is sized to fi t the right whale onto the page. Skeletons in the group on the upper right are scaled so that the distance between the shoulder and the hip joints are equal in all seven species. Thus, the body cavities of this group are approximately the same length. A reference line representing 1 m is given below each of these drawings; note that it is different for each skeleton in this scaling scheme. Both groups are sized so that the dolphins on the right and left are equal in length. Copyright S. A. Rommel.

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the three-toed sloth ( Bradypus ) has nine. Serial fusion (ankylosis) of two or more cervical vertebrae is common in cetaceans, but all cetaceans have seven cervical vertebrae. Contrary to what has been reported in some published works, the cervical vertebrae in some

cetaceans (e.g., the narwhal, beluga, and river dolphins) are unfused and provide considerable neck mobility.

The fi rst two cervical vertebrae are named the atlas (C1) and the axis (C2). Unlike all other vertebrae, the atlas and axis of most

Postzygapophyses(caudal articular facets,bottom or lateral aspect)

Transverseprocesses

Transverseprocess

Centra(Bodies)

Neural spines(spinous processes)

Intervertebral disk

(B)

(D)(C)

Annulusfibrosus

Nucleuspulposus

(A)

Prezygapophyses(cranial artir facets,culatop or medial aspect)

Intervertebral disks

T2 T5 T10

(cranialviews)

(Lateralviews)

(Lateralviews)

(Cranialviews)

(Dorsalview)(Dorsal

view)

(Lateralviews)

(Cranialviews)

(dorsalviews)

Neuralcanal

Neuralarch

Neuralspines

Figure 2 (A) Dorsal and lateral views of the manatee and its vertebrae. (B) Parts of a vertebra. The centrum (body) of each vertebra is the primary mechanical support of the vertebral column. Vertebral centra help prevent the body of the animal from collapsing when large body muscles contract. Dorsal to the centrum is an arch of bone, the neural arch; within the arch is the neural canal. The neural arch protects the spinal cord and it may extend dorsally as a neural spine (spinous process). (C) The fl exible region between adjacent centra functions as a tough joint, the intervertebral disk. These interver-tebral fi brocartilage joints have two parts: the inner nucleus pulposus and the outer annulus fi brosus. (D) Zygapophyses are articular facets that constrain motions between adjacent vertebrae. The cranial pair on each vertebra are prezygapophyses and the caudal pair are postzygapophyses. The region of articulation between prezygapophyses and postzygapophyses of adjacent vertebrae is typically a synovial joint if the facets overlap. In some regions of the vertebral column the facets do notoverlap and they may be connected by collagen fi bers. Copyright S. A. Rommel.

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Sternum 2–3 cartilagenoussternal ribs

Pelvic vestige

PubisVery largepresternal cartilage

Sternabrae

SternabraeVery largexiphoid cartilage

Acetabulum

Iliaccrest

PubisAcetabulum

Iliaccrest

Ischium

Ischium

Cartilagenoussternal ribs

Cartilagenoussternal ribs

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Ca25

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T15 L5

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Florida manateeC6:T17:L1:S0:Ca25

Harbor sealC7:T15:L5:S3:Ca9

California sea lionC7:T15:L5:S3:Ca14

SternumPelvic vestige

First chevronNo distinct sternal ribs

C7T14

L11

Ca26Northern right whaleC7:T14:L11:S0:Ca26

SternabraeBony sternal ribs Pelvic vestige

Firstchevron

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Ca26Bottlenose dolphin

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SternabraePubis

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Ischium

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C7

T14

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L5

Ca10

S6Polar bear

C7:T14:L5:S6:Ca10

Sternabrae Pubis

Acetabulum

Iliaccrest

Ischium

Cartilagenoussternal ribs

C7 L6

Ca15

S4Sea otter

C7:T14:L6:S4:Ca15

Figure 3 The axial skeletons plus pelves of the seven selected marine mammal species. There are typically fi ve separate vertebral regions: cervical, thoracic, lumbar, sacral, and caudal. In this illustration, each skull and vertebral column is scaled to similar shoulder–” hip ” dis-tances. Sacral vertebrae are, by defi nition, associated with an attached pelvis; therefore, the permanently aquatic species with (unattached) pelvic vestiges, have no sacral vertebrae. The permanently aquatic species (manatee, dolphin, and right whale) have pelvic vestiges. The ver-tebral formula, an alpha-numerical abbreviation for the numbers of vertebrae in each region is located below each common name; the num-bers given are for the specimens illustrated; some of these numbers vary between individuals of each species. Vertebral ribs extend from the vertebral column to join the sternal ribs, which extend from the sternum. The sternum develops from a series of sternebrae. In some species (e.g., humans, right whales, and manatees), the sternebrae fuse into a single bony unit. Copyright S. A. Rommel.

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mammals are not separated by an intervertebral disk but rather by a synovial joint, similar to the skull-atlas joint ( Fig. 4A ); the shapes of these fi rst two vertebral joints dictate the range of motion between the skull and the vertebral column. Typical skull motions on the atlas are up-and-down and side-to-side ( Fig. 4A ). The axis has an elon-gated centrum, the dens (odontoid process), which restricts motions between the atlas and axis to rotations. Test these constraints on yourself by bending and twisting your head and neck. Head nodding, as in expressing “ yes, ” is constrained by the skull-atlas joint; head rotations expressing “ no, ” are constrained by the atlas-axis joint.

Typically, the permanently aquatic marine mammals have rela-tively short necks; in contrast, the pinnipeds have relatively long necks. Comparison of the skeletons of the seal and sea lion reveals that they have similar neck lengths, although external appearance is very different. Seals often hold their heads close to the thorax, which causes the neck to form a deep “ S ” curve, providing them with a “ slingshot potential ” for grasping prey (or inattentive handlers).

Cervical vertebrae may have distinct transverse foramina that protect blood vessels when the neck is fl exed. Transverse foramina are particularly distinct in the cervical vertebrae of the carnivorous marine mammals. A pair of notches (or foramina) in the neural arch of the atlas may be present ( Fig. 4A ); these openings are for the fi rst spinal nerve pair that exits the neural canal between the back of the skull and the neural arch of C1. Rarely, one fi nds cervical ribs , which are moveable extensions of the ventral transverse processes; cervical ribs do not extend to the sternum.

D. Thoracic Region The thoracic region (thorax) is defi ned by the presence of more or

less movable (i.e., not fused to the respective vertebrae) ribs ( Figs 3, 4B ). The thoracic and lumbar vertebrae support the trunk. By defi ni-tion, the fi rst thoracic vertebra has a pair of ribs that, unlike cervical ribs, extend to the sternum. Most thoracic vertebrae have ribs that possess two segments. The proximal, dorsal segment is attached to the vertebral column and is termed a vertebral rib ( Fig. 3 ). A distal, ventral segment is attached to the sternum and is termed a sternalrib ( Romer and Parsons, 1986 ). A joint between the vertebral rib and sternal rib may help accommodate fl exibility of the thorax. The dis-tinction between vertebral and sternal ribs is more common in birds and some reptiles, but it is less common in mammals because most mammals have cartilaginous sternal ribs termed costal cartilages. We make this distinction because, unlike most other mammals, some odontocete cetaceans have bony rather than cartilaginous sternal ribs ( Rommel 1990 ; Cotten et al ., in press ).

As suggested above, the mechanics of motion of the thoracic vertebrae are different from those of either the cervical vertebrae or the post-thoracic vertebrae. Typically, the thorax is relatively more fl exible axially and laterally than dorsoventrally. Thoracic ver-tebrae have dual functions of longitudinal body support and (with their ribs) support of the respiratory muscles. This dual function is refl ected in the arrangement, size, and shape of the zygapophyses. The last thoracic vertebrae have ribs associated with them, but these last ribs may not be attached to their respective vertebrae, with lit-tle or no indication on their respective vertebrae to indicate their presence The attachment sites of ribs on the vertebrae are called rib facets (costal facets; ribs � costae) if the region of attachment has a distinct articulation ( Fig. 4B ). Rib facets may be located on the ver-tebral centrum, on the transverse processes, or on both. Some rib attachments are made via long connective-tissue fi bers; these ribs do not actually contact the respective vertebra, and there is no obvious structure on the (cleaned) vertebrae to suggest rib attachment. For this reason, dogmatic adherence to narrow defi nitions of numbers of thoracic or lumbar vertebrae, or both should be avoided. The ceta-ceans and pinnipeds have very mobile rib cages. Surprisingly, diving mammals have considerable dorso-cranial to ventro-caudal “ tilt ” to their ribs. In these species, the double-headed ribs (see below) have joints that are aligned to allow for substantial cranial to caudal swing of the attached vertebral ribs. This extreme mobility of the rib cage can help accommodate the lung volume changes that accompany changes in pressure with depth. It may also have evolved to accom-modate rib cage dynamics that occur during lung ventilation ( Cottenet al ., submitted ) caused when abdominal muscle contractions pre-vent caudal displacement of the diaphragm during inspiration; in this case ribs, could be moved forward to increase lung volume.

Some thoracic vertebrae have ventral vertebral projections called hypapophyses— not to be confused with chevron bones (chevrons typically span the intervertebral joints and are not parts of the verte-brae themselves; Figs. 3, 4C ). In the manatee, the central tendon of the diaphragm is fi rmly attached along the midline to hypapophyses. Hypapophyses also occur in some cetaceans (i.e., Kogia, the pygmy and dwarf sperm whales) in the caudal thorax and cranial lumbar regions; these hypapophyses are associated with the diaphragm.

Thoracic neural spines are often longer than those in other regions of the body ( Figs. 3, 4 ) to provide mechanical advantage for neck mus-cles. Interestingly, terrestrial species with large heads tend to have long neural spines; however, the buoyancy of water may negate the need for such long neural spines in the marine mammals—contrast the animals that come onto land with the fully aquatic ones in this regard.

Figure 4 (A) The cervical vertebrae. At the top of this illustration, these vertebrae are fi lled in on the dorsal and lateral views of the mana-tee skeleton. The fi rst and second cervical vertebrae are named the atlas and the axis, respectively. Cervical vertebrae may have transverse foramina, which perforate the bases of the transverse processes. Typical skull motions on the atlas are up-and-down and side-to-side. The axis has an elongated centrum, the dens, which extends into the large neural canal of the atlas. The shape of the dens restricts motions between the fi rst two vertebrae to rotations parallel to the long axis of the body. (B) Thoraco-lumbar vertebrae. Thoracic vertebrae support the ribs, which anchor the diaphragm muscles. Some ribs are double headed and articulate with their respective vertebrae via capitula and tubercula. Each capitulum articulates with one or more costal facets on the vertebral centrum at or near the intervertebral disk. Each tuberculum artic-ulates with a facet on the transverse process of its respective vertebra. Lumbar vertebrae are trunk vertebrae without ribs—instead they have pronounced transverse processes. In manatees there may be a rib on one side and a transverse process on the other side of the same lumbar vertebra. (C) Caudal vertebrae are found in the tail. At the top of this illustration, these vertebrae are fi lled in on the dorsal and lateral views of the manatee skeleton. In the permanently aquatic marine mammals that have no direct attachment between the pelvic vestiges and the vertebral column, the transition between lumbar and caudal vertebrae is defi ned by the presence of chevron bones. The chevron bones are ventral intervertebral ossifi cations. By defi nition, each chevron is associated with the vertebra cranial to it. Copyright S. A. Rommel.

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Ribs and transverse processes are homologous structures, but the presence of a movable joint ultimately distinguishes a rib from a transverse process in an adult. An “ unfi nished ” joint may be indica-tive of developmental age; in manatees, there may be a movable “ riblet ” (pleurapophysis, pleura � side or rib) on one side and an attached “ transverse process ” on the other side of the same (typi-cally the fi rst lumbar) vertebra. Pleurapophyses are more common in some of the lower vertebrates ( Romer and Parsons, 1986 ; Kardong, 1998 ).

A rib may attach to its respective vertebra ( Fig. 4B ) at one or more locations. Typically the fi rst few ribs are “ double-headed ” and have two distinct articulations with their juxtaposed vertebrae. The cranial-most articular part of a double-headed rib is the capitulum(plural, capitula) or head, and it articulates (via a synovial joint) with the body (or bodies) of one or two vertebrae. The tuberculum (plu-ral, tubercula) is the second attachment site of a double-headed rib; it articulates (either with a synovial joint or by connective tissue fi bers) to a transverse process of the respective vertebra. Since the capitula of some double-headed ribs touch two vertebrae, the ver-tebra with the transverse process attachment is used to identify the respective vertebra.

The caudal-most ribs have single attachments and are referred to as “ single-headed ” . In most mammals, the single-headed ribs have lost their tubercula and are attached to their respective vertebrae by the capitulum at the centrum. In contrast, the single-headed ribs of cetaceans lose their capitula and are attached to their respective verte-brae by their tubercula at the transverse processes ( Rommel, 1990) , as occurs in some reptiles. The transverse processes of cetacean thoracic vertebrae may be longer than those of other mammals. Thus, the sin-gle-headed ribs of cetaceans attach to the vertebrae farther from the midline than do the single-headed ribs of other mammals. The last ribs often “ fl oat ” free at one or both ends, that is, they are attached to neither their associated vertebra nor the sternum.

E. Sternum Embryonically, the sternum is formed from serial elements,

called sternebrae (the sternal equivalent of vertebrae, Fig. 3 ). The fi rst and last sternebrae are called the manubrium and xiphisternum , respectively. In some odontocetes, all mysticetes, and all sirenians, the sternebrae fuse into a single unit. Sternal ribs extend from the sternum to join the vertebral ribs. Seals have an elongated prester-nal cartilage extending cranially from the manubrium; some taxa, particularly the sea lion, have an enlarged post-sternal cartilaginous extension, the xiphoid cartilage .

F. Lumbar Region The lumbar vertebrae are trunk vertebrae that typically do not bear

movable ribs ( Fig. 3 ). Recall that ribs and transverse processes develop from homologous embryonic structures. Occasionally, a distinct pleu-rapophysis may be found in this region. As noted above, pleurapophy-sis are commonly found in manatees; these “ lumbar ribs ” are clearly distinct from thoracic ribs ( Fig. 4B ). Typically, the lumbar vertebrae are more fl exible dorsoventrally than they are laterally and they may have no axial fl exibility. Some of the mobility of the lumbar vertebrae may be constrained by the ribs in front of them.

As already noted, the number of lumbar vertebrae is usually closely linked to the number of thoracic vertebrae; an increase in number in one section typically means a reduction in the other. For example, there are 19 thoraco-lumbar vertebrae in all species of

Artiodactyla, whereas there are 20 or 21 in the Carnivora; compare these numbers with those of the selected marine mammals ( Fig. 3 ).

G. Sacral Region There are at least two commonly accepted defi nitions for sac-

ral vertebrae: (a) serial fusion of post-lumbar vertebrae, only some of which may attach to the ileum of the pelvis and (b) only those vertebrae that attach to the ileum, whether or not they are serially fused. Both defi nitions have merit. In species where there is contact between the vertebral column and the pelvis, it is relatively easy to defi ne sacral vertebrae. However, it is not easy in the cetaceans and manatees because there is no direct attachment between the pel-vic vestige and the vertebral column and there are no serially fused vertebrae in this region (dugongs have a ligamentous attachment between the vertebral column and the pelvic vestiges). Thus, most of the permanently aquatic species have, by either defi nition, no sac-ral vertebrae. In other mammals, the number of sacral vertebrae is commonly 2–5. Within a species, the number of serially ankylosed vertebrae may vary, particularly with age.

H. Caudal Region Caudal (cauda � tail) vertebrae are found in the tail ( Figs. 3, 4C ).

The number of caudal vertebrae varies widely. Long tails usually require numerous caudal vertebrae. Florida manatees have between 22 and 27 caudal vertebrae, and bottlenose dolphins 25–28—for ceta-ceans, the minimum is 13 in Caperea marginata (pygmy right whale); the maximum is 49 in Phocaenoides dalli (Dall’s porpoise). Note that the caudal vertebrae of cetaceans extend to the tip of the tail (fl uke notch), whereas manatee vertebrae stop 3–9 % of the total body length from the fl uke tip ( Fig. 1 ). Caudal vertebrae range from being robust, important locomotory structures in the permanently aquatic species, to being relatively small vertebrae in the pinnipeds and polar bear.

I. Chevron Bones The chevron bones or chevrons ( Fig. 4C ) are ventral interverte-

bral ossifi cations found only in the caudal region. They are relatively large in the permanently aquatic species but can be found as small ossifi cations in many other species, including the dog. Chevrons function to increase the mechanical advantage of the hypaxial mus-cles to fl ex the tail ventrally. By defi nition, each chevron is associated with the vertebra cranial to it (note that there is some controversy over which is the “ fi rst ” caudal Rommel 1990 ). Pairs of chevron bones form arches, creating a ventral channel called the hemal canal. Within the hemal canal, the blood vessels (caudal arteries and veins) that supply the tail are protected. In sirenians and some cetaceans the chevron bone pairs fuse at the ventral midline.

II. Appendicular Skeleton A. Pectoral Limb Complex

The forelimb ( Fig. 5 ) is referred to as a fl ipper in the perma-nently aquatic species (in true seals and sea lions the hindlimb is also referred to as a fl ipper). The forelimb includes the scapula, humerus, radius and ulna, the multiple bones of the manus, and the clavicle.

The scapula is attached to the axial skeleton only by mus-cles; there is no functional clavicle in the marine mammals ( Klimaet al., 1980 ; Strickler, 1978 ). The scapula consists of an essentially fl at (slightly concave medially) blade with an elongate scapular spineextending laterally from it. The distal tip of the spine is the acromion .

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The scapular spine is roughly in the center of the scapular blade in most mammals. However, in cetaceans and manatees, the scapular spine is close to the cranial margin of the scapular blade, and its acromion process extends beyond the leading edge of the blade.

The proximal humerus has a ball-and-socket articulation in the gle-noid fossa of the scapula; this is a relatively fl exible joint. The humerus

articulates distally with the radius and ulna; this is also a fl exible joint in most mammals, but it is mechanically constrained in cetaceans. The olecranon is a proximal extension of the ulna that increases the mechanical advantage of the triceps muscles, which extend the fore-limb. In species like the polar bear and the sea lion, the olecranon is robust; however, in cetaceans it is relatively small. The radius and ulna

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Figure 5 The forelimb (pectoral appendage) includes the humerus, radius and ulna, and manus. The forelimb attaches to the pecto-ral girdle which is made of bilaterally paired scapulae. The scapula is a fl at (slightly concave medially) blade with an elongated scapu-lar spine extending laterally from it. The distal tip of the spine is the acromion process. The humerus has a ball-and-socket articulationwith the glenoid fossa of the scapula. The humerus articulates with the radius and ulna at the elbow. The radius and ulna articulatewith the proximal aspect of the manus at the wrist. The manus includes the carpals, metacarpals, and phalanges. There are fi ve “ col-umns ” of phalanges, each “ column ” is called a digit. The digits are numbered, using Roman numerals, starting from the cranial aspect (associated with the radius, in humans—the thumb). Copyright S. A. Rommel.

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of manatees fuse at both ends as the animal ages. This fusion prevents axial twists that pronate and supinate the manus. The cetacean radius and ulna are also mechanically constrained by the surrounding con-nective tissues but are not typically fused. The forelimbs of the sea otter are very mobile allowing for the manipulation of food.

The distal radius and ulna articulate with the proximal aspect of the manus. The manus includes the carpals, metacarpals, and phalanges.

There are fi ve “ columns ” of phalanges, each of which is called a digit. The digits are numbered, using Roman numerals, starting from the cranial aspect (the thumb; associated with the radius). Note that the longest digit may be different in the different species ( Fig. 6 ).

In many of the marine mammals, the “ long ” bones of the pec-toral limb (humerus, radius, and ulna) are relatively short, and the phalanges are elongated. Cetaceans are unique among mammals in

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Figure 6 The pelvic appendage (hind limb) and pelvic girdle. The typical mammalian pelvis is made of bilaterally paired coxae attached to one or more sacral vertebrae. Each coxa is made of three elements: the ilium, ischium, and pubis. The crest of the ilium is a prominent landmark; it fl ares forward and outward beyond the region of attachment between the sacrum and the ilium. The two halves of the pelvis join at the ventral midline pubic symphysis. In the permanently aquatic marine mammals there is only a vestige of a pelvis. The hindlimb, if present, is attached to the pelvic girdle via a ball (femoral head) and socket (acetabulum) joint at the hip. The proximal limb bone is the femur. Distally, the femur articulates with the tibia and the fi bula at the knee joint. The tibia and fi bula distally articu-late with the pes at the ankle. Note that the pes is oriented in different “ planes ” in some of the selected species. The pes consists of the tarsals proximally, the metatarsals medially, and the phalanges distally. Copyright S. A. Rommel.

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that they have more phalanges than do any of the other mammals ( Fig. 6 ); this condition is known as hyperphalangy ( Howell 1930 , Cooper et al., 2007 ). The number varies between individuals of each species—the pilot whale has the most (14), the bottlenose dolphin has a maximum of 9, and the right whale has a maximum of 7.

Notice the “ plane ” in which each manus is oriented ( Fig. 6 ). The sea otter’s manus, much like that of humans, is very dexterous. The polar bear manus, much like that of the dog and other terrestrial quadrupeds, is more dexterous. The permanently aquatic species hold the manus roughly parallel to the midsagittal plane of the body or parallel to the nearest body surface.

B. Pelvic Limb Complex The typical mammalian pelvis is made of bilaterally paired bones:

ilium, ischium, and pubis ( Fig. 7 ). Each half of the pelvis attaches (via the ilium) to one or more sacral vertebrae; the attachment may vary from simple apposition in juveniles to fusion in adults. The crest of the ilium, which is a prominent landmark, fl ares forward and out-ward beyond the region of attachment between the sacrum and the

ilium. The two halves of the pelvis join at the pubic symphysis on the ventral midline. In the permanently aquatic marine mammals, there is only a vestige of a pelvis to which portions of the rectus muscles of the abdomen may attach; the male reproductive organs may be sup-ported by these vestiges as well ( Pabst et al ., 1998 ). Occasionally, in some of the large whales, a non-functional hindlimb rudiment artic-ulates with the pelvic vestige.

The hindlimb, if present, is attached to the pelvis via a ball and socket joint at the hip. The proximal limb bone is the femur, whose head articulates with the socket of the pelvis, the acetabulum. Distally the femur articulates with the tibia and the fi bula at the knee. The tibia and fi bula articulate distally with the pes or foot at the ankle ( Fig. 7 ). The pes is composed of the proximal tarsals, the medial metatarsals, and the distal phalanges. Note that the digits of the sea lion terminate a signifi cant distance from the tips of the fl ip-per. Of the chosen group of marine mammals, the limbs of the polar bear are closest in gross appearance to those of the terrestrial mam-mals. In contrast, many of the other marine mammals have rela-tively short “ long ” bones (femur, tibia, and fi bula) and relatively long

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Figure 7 (A) Postcranial features that change with age. Some post-cranial elements grow in length by separate ossifi cation centers, the epiphyses, at the margins of the bony element. The humeral head and distal humerus develop as epiphyses (fi lled parts in illustra-tion). Patterns of fusion of these epiphyses provide information about aging. The epiphyses illustrated here have been used for relative aging of manatees and dolphins. (B) Non-epiphyseal sutures also indicate age in the postcranial skeleton. The transverse processes and the neural arches have sutures that disappear early in adolescence. In addition, the two halves of the neural arch ankylose at the dor-sal midline to the base of the neural spine. (C) Epiphyses may occur on the ends of ribs and the tips of transverse processes and neural spines. Most mammals have distinct vertebral epiphyses at each end of their growing vertebrae. Vertebral epiphyses fuse to theirrespective vertebral centra at physical maturity of the vertebra. Copyright S. A. Rommel.

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phalanges. The femurs of some phocids (e.g., the harbor seal) are so short that the knee cannot contact the ground.

Note that the pes is oriented in different “ planes ” in some of the selected species ( Fig. 7 ). The pes of the polar bear is oriented in a fashion similar to that of the dog. The sea otter, seal, and sea lion all orient the pes parallel to the sagittal plane when swimming. The sea lion can rotate its pelvis and hind fl ippers to “ walk ” on land, and the sea otter can manipulate its hind fl ippers to hold food. Compare the positions of the fi rst and last digits in the sea otter with those of the seal and sea lion, and note how the sea otter’s fi bula crosses the tibia to achieve this orientation.

C. Sexual Dimorphisms In many mammals the adult males are larger than the adult

females, and among marine mammals, this dimorphism is extremely pronounced in certain pinnipeds and the sperm whales. In contrast, in baleen whales and some other species the adult females are larger than the adult males. In the permanently aquatic marine mammals, there may be sexual dimorphisms in the pelvic vestiges ( Fagone et al., 2000 ). The penises of mammals are supported by tough fi brous struc-tures, the crura, which attach to the pubic bones of the pelvis. The muscles that engorge the penis with blood are also attached to the pel-vis, and presumably the mechanical forces associated with these mus-cles infl uence pelvic vestige size and shape, particularly in manatees. Males in some groups of mammals, particularly the carnivores, have a bone within the penis (the baculum or os penis) that helps support the penis.

III. Sutures and Epiphyses Many bony features change in size and shape as the individual

develops and matures; these features can be used as milestones in life history studies, and in some cases, they can be fairly accurate estimators of age. Some postcranial elements grow from separate ossifi cation centers at the margins of the bones ( Fig. 7A ). Epiphyses(epi- , upon, and physis- , grow or generate) are regions at the ends of bones (most often at or near a joint) associated with longitudinal growth in mammals. Epiphyses allow the portion of the bone near a joint to grow at a different rate than the rest of the bone and allow new bone to be laid down away from the articulating surface. Growth occurs at a cartilaginous plate between the epiphysis and the dia-physis ( dia- , between; body or shaft). At the completion of growth, the epiphysis fuses with the rest of the bone, and the cartilage plate disappears. Eventually the suture between the two parts also disap-pears. Because most marine mammals are large, their epiphyses are more evident than those of the smaller terrestrial mammals.

The best-studied epiphyses are those of the long bones. There are, however, other epiphyses that are less well known. For example, the proximal fi nger bones may have epiphyses ( Fig. 7B ). The pattern of epiphysial fusion in the fl ipper can be used to determine relative age of an individual, when compared to the fusion pattern in other animals of known age. Occasionally epiphyses are found on the prox-imal ends of ribs, on the scapula located at or near the coracoid ( Fig.7A ), or on the tips of neural spines and transverse processes.

Among the epiphyses most important to mammalian osteologists are those located at each end of the vertebral centrum ( Fig. 7C ). Most mammals have distinct bony plates at each end of their grow-ing vertebrae. These plates are vertebral epiphyses. Manatees (and humans) are among the few species of mammals that have indistinct or no vertebral epiphyses. In manatees, the vertebral epiphyses are

delicate irregular fi lms of bony tissue found within the cartilaginous surfaces at the cranial and caudal ends of the centrum. After these epiphyseal sutures are completely fused, the skeleton cannot grow in length and the individual is considered skeletally mature. Skeletal maturity may or may not coincide with other forms of maturity, such as reproductive maturity.

Non-epiphyseal sutures can also be used to estimate age of parts of the postcranial skeleton ( Fig. 7C )—for example, the two halves of the neural arch ankylose at the dorsal midline to form the base of the neural spine. These sutures may persist well into adulthood in cetaceans.

There is much more to learn about the postcranial skeleton. Consult Pabst et al. (1999) for additional functional morphology on marine mammals, Young (1975) for information on mammals in gen-eral, and Alexander (1994) for vertebrates. For principles on size and scaling try Calder (1966) and Schmidt-Nielsen (1984) .

See Also the Following Articles Skull Anatomy ■ Forelimb ■ Hind Limb Anatomy

References Alexander , R. McN ( 1994 ). “ Bones: The Unity of Form and Function . ”

Macmillan , New York . Calder , W. A. , III ( 1966 ). “ Size, Function, and Life History . ” Dover

Publications, Inc , Mineola, NY . Cooper , L. N. , Berta , A. , Dawson , S. D. , and Reidenberg , J. S. ( 2007 ).

Evolution of hyperphalangy and digit reduction in the cetacean manus . Anat. Rec. 290 , 654 – 672 .

Cotten, P. B., Piscitelli, M. A., McLellan, W. A., Rommel, S. A., Dearolf, J. L., and Pabst, D. A. Submitted (In press). The gross morphology and histochemistry of respiratory muscles in bottlenose dolphins, Tursiops truncatus. J. Morphol .

Evans , H. E. ( 1993 ). “ Miller’s Anatomy of the Dog , ” 3rd ed. W. B. Saunders Company , Philadelphia, PA .

Fagone, D. M., Rommel, S. A., and Bolen, M. E. (2000). In press. Sexual dimorphism in vestigial pelvic bones of the Florida manatee. FloridaScientist 63(3), 177–181.

Flower , W. H. ( 1885 ). “ An Introduction to the Osteology of the Mammalia , ” 3rd ed . Macmillan and Co , London (reprinted by A. Asher & Co., Amsterdam, 1966) .

Flower , W. H. , and Lydekker , R. ( 1891 ). “ An Introduction to the Study of Mammals Living and Extinct . ” Adam and Charles Black , London .

Giffen , E. B. ( 1992 ). Functional implications of neural canal anatomy in recent and fossil marine carnivores . J. Morphol. 214 , 357 – 374 .

Howell , A. B. ( 1930 ). “ Aquatic Mammals: Their Adaptions to life in the water . ” Charles C. Thomas , Springfi eld, IL .

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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