THE ANATOMICAL RECORD 294:1743–1756 (2011)

Development of the Skull of thePantropical Spotted Dolphin (Stenella

attenuata)MEGHAN M. MORAN,1* SIRPA NUMMELA,2 AND J.G.M. THEWISSEN1

1Department of Anatomy and Neurobiology, Northeastern Ohio Universities Colleges ofMedicine and Pharmacy, Rootstown, Ohio

2Department of Biosciences, University of Helsinki, Helsinki, Finland

ABSTRACTWe describe the bony and cartilaginous structures of five fetal skulls

of Stenella attenuata (pantropical spotted dolphin) specimens. The speci-mens represent early fetal life as suggested by the presence of rostral tac-tile hairs and the beginnings of skin pigmentation. These specimensexhibit the developmental order of ossification of the intramembranousand endochondral elements of the cranium as well as the functional andmorphological development of specific cetacean anatomical adaptations.Detailed observations are presented on telescoping, nasal anatomy, andmiddle ear anatomy. The development of the middle ear ossicles, ectotym-panic bone, and median nasal cartilage is of interest because in the adultthese structures are morphologically different from those in land mam-mals. We follow specific cetacean morphological characteristics throughfetal development to provide insight into the form and function of thecetacean body plan. Combining these data with fossil evidence, it is possi-ble to overlie ontogenetic patterns and discern evolutionary patterns ofthe cetacean skull. Anat Rec, 294:1743–1756, 2011. VVC 2011 Wiley-Liss, Inc.

Keywords: cranial development; Stenella attenuata; telescoping;middle ear; Cetacea

The development of the Cetacea skull was studied inembryos (de Burlet, 1913a, 1913b, 1914a, 1914b;Schreiber, 1916; Honigmann, 1917; Rauschmann et al.,2006; Thewissen and Heyning, 2007) and fetuses(Schulte, 1916; Ridewood, 1923; Eales, 1950). Cetaceanresearch focused on specific biological systems to under-stand differences within Mammalia. Comtesse-Weidner(2007), Miller (1923) and Kellogg (1928a, 1928b) studiedmorphological elements including telescoping. Oelschl-ager and Buhl (1985), Klima and van Bree (1990), andKlima (1995, 1999) studied nasal anatomy and develop-ment. Oelschlager (1986, 1990), Solntseva (1990, 1999,2002), and Kinkel et al. (2001) concentrated on hearingreception and sound emission while Mead and Fordyce(2009) focused on general skull anatomy. Although com-parative embryological studies on cetaceans were rare,developmental studies were mostly nonexistent. Suchstudies (e.g., Thewissen et al., 2006, Armfield et al., inpress) allow for a deeper understanding of the ontoge-netic constraints on the evolution of the cetacean bodyplan.

Habitat changes alter adaptations for specific cetaceanbody plans. These modifications include those of anatom-ical function and body plan from land mammals to fullyaquatic, air breathing marine mammals. Our studyfocuses on anatomical structures of five Stenella attenu-ata (pantropical spotted dolphin) fetuses. Here wedescribe bony and cartilaginous structures of the

Grant sponsor: National Science Foundation (J.G.M.T.);Grant number: 34284; Grant sponsor: Academy of Finland(S.N.); Grant number: 120682.

*Correspondence to: Meghan M. Moran, Department of Anat-omy and Neurobiology, 4209 State Route 44, P.O. Box 95,Northeastern Ohio Universities Colleges of Medicine and Phar-macy, Rootstown, OH 44272. Fax: þ1-330-325-5911. E-mail:mmoran1@neoucom.edu

Received 18 May 2010; Accepted 22 December 2010

DOI 10.1002/ar.21388Published online 8 September 2011 in Wiley Online Library(wileyonlinelibrary.com).

VVC 2011 WILEY-LISS, INC.

Fig. 1. Five cleared and stained pantropical spotted dolphin (Stenella attenuata) fetuses. Alcian bluestains the cartilage and Alizarin red stains the bone. Specimen numbers are listed to the left of each fe-tus. LACM 94671 is early stage 20, TL: 85 mm. LACM 94592 is late stage 20, TL: 155 mm. LACM 94310is stage 21/22, TL: 185 mm. LACM 94285 is stage 23, TL: 213 mm. LACM 94382 is stage 23, TL: 225mm. Scale bar ¼ 1 cm.

TABLE 1. Stenella attenuata fetal specimen details

Specimen number Stage Approximate age Total length (TL) Skull length

94671 C20 � 70 days 85 2094592 C20 80–110 days 155 3794310 C21/22 80–110 days 185 4594285 C23 110–120 days 213 5694382 C23 110–120 days 225 58

Specimen numbers, expanded Carnegie stage, associated ages, as well as average body length and average skull length inmillimeters (based on Sterba et al., 2000).

1744 MORAN ET AL.

cranium of these fetuses to elucidate telescoping, nasalanatomy, and ear anatomy.

MATERIALS AND METHODS

We describe the skulls of five S. attenuata fetusesfrom the Natural History Museum of Los AngelesCounty (LACM) in Los Angeles, CA (Fig. 1). Thesefetuses are staged using the adapted and expandedCarnegie system from Thewissen and Heyning (2007).Ages of fetuses are based on Sterba et al. (2000).The five specimens are: LACM 94671, LACM 94592,LACM 94310, LACM 94285, and LACM 94382 (Fig. 1and Table 1).

Each fetus is measured by placing a piece of stringalong the dorsum of the fetus from the rostral tip to thetail tip for a total length (TL) measurement (Table 1).The skull length is measured using calipers (Table 1)from the tip of the rostrum to the caudal most extent ofthe occipital bones and cartilage. Each measurement istaken three times and the average is listed in this table.No linear measurements of individual bones are pre-sented because the vast shape change of cranial bonesduring development makes it difficult to take measure-ments consistently.

Each Stenella fetus is cleared and stained (Wassersug,1976) to show only bone and cartilage structures. Othersoft tissue structures are obliterated during the stainingprocess. The specimen is skinned, eviscerated, andwashed in water for about 7 days to remove fixative.The head is bisected to allow for better visualization ofthe cranial bones and cartilaginous areas after staining.This also allows for further molecular study to be com-pleted on the contralateral side of each fetal skull speci-men. Symmetry was not addressed during cranialdevelopment because this technique made it impossible.The water is changed every day to maximize the wash-ing process. The fetus is then put into a 40% acetic acid/60% alcohol solution for 7 days. Again, the solution ischanged every day. After 7 days in the 40% acetic acid/60% alcohol solution, the solution is replaced and Alcianblue stain is added to the solution. The Alcian bluestain/acetic acid/alcohol solution is checked every day;the solution is replaced every 2�3 days for anywherebetween 5 days to 4 weeks depending on how well thespecimen absorbs the stain. The Alcian blue stains thecartilaginous structures of the specimen.

Once the blue stain is absorbed by the cartilage, thespecimen is placed in a 3–5% potassium hydroxide/Aliza-rin red stain solution for 1 day or until the bone absorbsthe red stain. This solution is checked every hour to pre-vent any damage the specimen because this solution isextremely caustic and tissue quickly deteriorates. TheAlizarin red stains the bone red. The double stained dol-phin fetus is placed into a series of rinses of increasingconcentrations of glycerol from 25% to 100%. Each fetusis stored in 100% glycerol in the refrigerator (4�C).Slight differences in the timing of these steps may occurbecause of the duration of fixation of the tissue.

RESULTS

Plates for LACM 94671 are provided in Figs. 1, 2, 3,and 4; LACM 94592 in Figs. 1, 3, 4, and 5; LACM 94310

in Figs. 1 and 6; LACM 94285 in Figs. 1 and 7; andLACM 94382 in Fig. 1.

Early Carnegie Stage 20

Intramembranous elements. The premaxilla(Pmx) is an elongated bone, constricted to a narrowwaist near its middle (Figs. 2A,D and 3A,B). The leftand right premaxillae (Fig. 2A and D) are wedgedbetween the left and right maxillae (Max, Figs. 2B,Dand 3A,B) and do not extend into the rostrum. The ros-trum lacks much ossification at this time. The premax-illa reaches farther rostrally than the maxilla. A smalland dense piece of premaxillary cartilage (Pmx crt) islocated at the tip of the rostrum (Figs. 2A,B and 3A,B).The external bony nares (Ebn, Fig. 2A) is caudal to thepremaxilla, high on the forehead. Medial to the premax-illa, a number of cartilaginous structures are associatedwith the nasal cartilage and vomer. The development ofthese structures has been described in some detail byKlima (1999) and will not be discussed here.

The maxilla (Figs. 2B,D and 3A,B) is a triangularbone on the lateral side of the face and forms a narrowportion of the palate. The maxilla forms most of the ros-trum at this stage. The caudal aspect of the maxilla islocated lateral to the cribriform plate (Cbp, Figs. 2A and3B) and the nasal cartilages. The maxilla extends dor-sally but not as far as the frontal (Fro) and parietal(Par) bones (Figs. 2B and 3A). Medially, the maxilla isgently concave and helps support the well-developed me-dian nasal cartilage (Nas crt, Figs. 2A and 3B) or meso-rostral cartilage (see Mead and Fordyce, 2009).

Posterior to the maxilla, the lacrimal (Lac, Figs. 2Dand 3A) is a narrow splint of bone in the anterior edgeof the orbit. In the wall of the pharynx, two ossificationcenters are posterior to the maxilla. The more anteriorof the two ossifications is the palatine (Pal, Figs. 2A and3B), which makes up the lateral wall of the nasopharyn-geal duct. Caudal to the palatine is the pterygoid bone(Ptg, Figs. 2A and 3B), which extends more ventrallythan the palatine. The vomer (Vom) is located mediallyto the palatine and the pterygoid (Fig. 3B).

The frontal bone (Figs. 2B,D,E and 3A,B) is a flat, rec-tangular bone that forms the ventrally concave edge ofthe dorsal orbit. The frontal bone does not extend intothe roof of the orbit and does not overlap with any otherbones in this specimen (Figs. 2B and 3A). The parietalbone (Par, Figs. 2B,D and 3A) is a flat, teardrop-shapedbone immediately caudal to the frontal bone and dorsalto the otic capsule (Otc, Figs. 2A,B,E and 3A). The squa-mosal bone (Squ, Figs. 2B,D and 3A) is a small bonelocated over the posterior end of Meckel’s cartilage, adja-cent to the otic capsule (Mec, Figs. 2A,B,D and 3A,B).

The dentary at this stage is ossified from the ramusthrough the central part of the dentary (Den, Figs.2A,B,D and 3A,B). This ossification starts at the anterioredge of Meckel’s cartilage near the tip of the rostrumand ends near the middle of the orbit. The dentary isconcave medially, enveloping Meckel’s cartilage andwrapping around it ventrolaterally. The ectotympanic(Ect) is a very thin horseshoe-shaped ossification locatedventral to the squamosal bone (Fig. 2D) and inferior tothe posterior end of Meckel’s cartilage.

DEVELOPMENT OF THE SKULL OF S. attenuata 1745

Fig. 2. Head of fetus LACM 94671 (TL: 85 mm), A: median. B: lat-eral. C: before clearing and staining; the soft tissue structures are insitu such as the brain, epiglottis, and the tongue. D: Close up of thecranium from an inferior–lateral orientation. E: Superior–medial view ofthe median cranial structures. Specific cartilaginous and bony featuresare labeled in the figure. Scale bar ¼ 5 mm for A–C and E. Scale doesnot apply to D which is foreshortened. Abbreviations in Figs. 2–7: Acc,accessory ossicle; Alg, alveolar groove; Alo, ala orbitalis; Alt, Ala tem-poralis; Bas crt, basihyoid cartilage; Boc, basioccipital bone; Boc crt,basioccipital cartilage; Bsp, basisphenoid bone; Bsp crt, basisphenoidcartilage; Cbp, cribriform plate; Crb, crus breve of the incus; Crl, cruslongum of the incus; Den, dentary bone; Ebn, external bony nares; Ect,ectotympanic bone; End for, endolymphatic foramen; Epi, epiglottis;Exo, exoccipital bone; Fro, frontal bone; Hyp, hypoglossal canal; Iam,

internal auditory meatus; Inc, incus; Inp, interparietal bone; Jfr, jugularforamen; Jug, jugal bone; Lac, lacrimal bone; LSoc, left ossification ofthe supraoccipital bone; Mal, malleus; Man, manubrium of the malleus;Max, maxillary bone; Mec, Meckel’s cartilage; Nas, nasal bone; Nas crt,nasal cartilage; Occ fis, occipitocapsular fissure; Opt for, optic foramen;Orb fis, orbitonasal fissure; Orb sph, orbitosphenoid; Otc, otic capsule;Pal, palatine bone; Par, parietal bone; Pmx, premaxillary bone; Pmx crt,premaxillary cartilage; Pop, posterior orbital process; Pre, presphenoidbone; Pre crt, presphenoid cartilage; Prl, pars lateralis of the squamosalbone; Prm, pars medialis of the squamosal bone; Ptg, pterygoid bone;RSoc, right ossification of the supraoccipital bone; Soc, supraoccipitalbone; Sph fis, sphenorbital fissure; Squ, squamosal bone; Sth, stylo-hyoid bone; Sth crt, stylohyoid cartilage; Stp, stapes; Thh, thyrohyoidbone; Thh crt, thyrohyoid cartilage; Ton, tongue; Vom, vomer bone.

Endochondral elements. The nasal capsule formsthe rostral wall of the cranial cavity. The cribriformplate is perforated by a large bilateral foramina for cra-nial nerve I (CN I) immediately lateral to the midline.Projecting rostrally in the midline is the large mediannasal cartilage (Nas crt, Figs. 2A and 3B), rostrum nasicartilagineum of Klima (1995, 1999). The lateral wall of

the nasal capsule is barely developed, consisting only ofa few isolated pieces of cartilage. The ethmoid isbounded caudally by the large orbitonasal fissure (Orbfis, Figs. 2A,B and 3B). Dorsal to the orbitonasal fissure,a thin cartilaginous process connects the nasal capsuleto the ala orbitalis (Alo, Figs. 2A,B,E and 3B). Such aprocess is not present in a 48 mm Phocoena (de Beer,

Fig. 3. Comprehensive black and white line drawings of the developing skulls of LACM 94671. A: Lat-eral, and B: medial views. LACM 94592, C: lateral and D: medial views. Some structures drawn here arenot represented in the photographs but were observed through the microscope. The course stipples rep-resent cartilage and the fine stipples represent bone.

DEVELOPMENT OF THE SKULL OF S. attenuata 1747

1937) but is present in a 92 mm Megaptera (Honigmann,1917). The ala orbitalis appears as a cartilaginous ringand is perforated by the optic foramen (Opt for, Figs.2A,B,E and 3A,B). This foramen is laterally placed andlarge as in the 48 mm Phocoena (de Beer, 1937), unlikethe 92 mm Megaptera (Honigmann, 1917). Caudally, theala orbitalis is separated from the ala temporalis(Alt, Fig. 2E) by the wide sphenorbital fissure (Sph fis,Figs. 2A,E and 3B). The ala temporalis extends fardorso-laterally to make up the lateral wall of thebraincase.

The median bones of the chondrocranium are not ossi-fied at this stage. The presphenoid cartilage (Pre crt,Figs. 2A and 3B) is thick, short, and fused along itsentire length with the ala orbitalis. The basisphenoidcartilage (Bsp crt, Figs. 2A and 3B) is thinner dorsoven-

trally and longer than the presphenoid cartilage. It iscontinuous with the basioccipital cartilage (Boc crt, Figs.2A and 3B). The median cartilages can also be seen inthe median view of the head before any staining wascompleted (Fig. 2C).

Dorsal to the foramen magnum is the supraoccipi-tal bone (Soc, Figs. 2A,B and 3A,B). The supraocci-pital bone is a small kidney-shaped ossification ofthe chondrocranium at the most posterior portion ofthe skull. The supraoccipital, exoccipital, and basioc-cipital are not ossified, but their cartilaginous pre-cursors form a complete caudal wall to the cranialcavity.

The otic capsule is large and reaches nearly to themidline (Otc, Figs. 2A,B,E and 3A). On the endocranialside, it has a separate foramen (internal auditory

Fig. 4. Close up views of the middle ear structures including ossicles. A: LACM 94671, B: black andwhite line drawing of LACM 94671, C: LACM 94592, D: black and white line drawing of LACM 94592.The course stipples represent cartilage and the fine stipples represent bone.

1748 MORAN ET AL.

meatus) for the facial and statoacoustic nerves. The in-ternal auditory meatus (Iam, Fig. 2E), and the large ba-sal whorl of the cochlea can be seen inside the oticcapsule. A small foramen pierces the otic capsule later-ally, and may represent the endolymphatic duct (End

for, Fig. 2E), as previously identified by de Beer (1937)in Phocoena. The occipital arch, the cartilaginous precur-sor to the exoccipital and basioccipital bones, makes upthe caudal part of the chondrocranium. The occipitalarch extends far dorsally and connects to the ala

Fig. 5. The head of LACM 94592 (TL: 155 mm). A: Medial. B: Lateral. C: Ventral oblique. D: Superior–lateral views. Scale bar ¼ 5 mm for A–D.

DEVELOPMENT OF THE SKULL OF S. attenuata 1749

temporalis in the lateral wall of the braincase. A largeoccipitocapsular fissure (de Beer, 1937) is located supe-rior to the otic capsule and ventral to the supraoccipitalbone separating the ala temporalis and the occipitalarch (Occ fis, Fig. 2A,E). The large, slit-like jugular

foramen (Jfr, Fig. 2E) separates the otic capsule fromthe occipital arch. Immediately caudal to the jugularforamen is the hypoglossal canal (Hyp, Fig. 2E), andimmediately medial to the jugular foramen is a smallforamen, possibly for the ventral petrosal sinus.

Fig. 6. The head of LACM 94310 (TL: 185 mm). A: Medial, B: Lateral, C: Dorsal, D: Superior–lateralorientation. Scale bar ¼ 1 cm for A–D.

1750 MORAN ET AL.

The middle ear ossicles are located caudal to Meckel’scartilage (Fig. 4A,B). The manubrium of the malleus(Man) is continuous with Meckel’s cartilage (Fig. 4A,B).The manubrium of the malleus is large, well-developed,and points ventrally. The incus (Inc) is caudal to the mal-

leus (Figs. 3A and 4A,B). The crus longum (Crl) of theincus points ventrally, and the crus breve (Crb) pointscaudally (Fig. 4A,B). The crus longum is slightly thickerthan the crus breve. The stapes is faintly visible orientedmediolaterally between the crus longum and otic capsule.

Fig. 7. The head of LACM 94285 (TL: 213 mm). A: Median. B: Lateral. C: Dorsal. D: Inferior–lateralorientation. Scale bar ¼ 1 cm for A–C. Scale bar ¼ 2 cm for D.

DEVELOPMENT OF THE SKULL OF S. attenuata 1751

Meckel’s cartilage (Mec) is a solid structure sur-rounded by the dentary (Figs. 2A,B,D, 3A,B, and 4A,B).Meckel’s cartilage projects rostrally and ventrally to thesquamosal bone (Fig. 2B). Near its rostral extremity, thecartilage fades where it is in close contact with the ossi-fying dentary.

The stylohyoid (Sth crt) and the thyrohyoid (Thh crt)cartilages are two bars of cartilage ventral to Meckel’scartilage (Figs. 2B,D, 3A,B, and 4A,B). The stylohyoidprojects as a straight cartilage bar from the chondrocra-nium. Ventrally, the stylohyoid cartilage is connected tothe basihyoid cartilage, which was damaged duringpreparation of this specimen. The thyrohyoid is a narrowbar of cartilage that projects caudally from this area to-ward the laryngeal cartilages. No ossification centers arepresent in the hyoid at this stage.

Late Carnegie Stage 20 and Stage 21/22

Intramembranous elements. The premaxilla(Pmx, Figs. 3D, 5A,D, and 6D) extends into the rostrumbut does not reach into the tip as a small remnant of thepremaxillary cartilage remains (Pmx crt, Figs. 5B and6A,B,D). Caudally, the dorsal aspect of the premaxilla isperforated by a foramen, presumably for a branch of theinfraorbital nerve and its associated vessels. Caudallythe premaxilla ends in a narrow process, rostral to theexternal bony nares (Ebn, Figs. 5A and 6A). The pre-maxilla is not fused to the maxilla but these two bonesare adjacent to each other.

The maxilla (Max) is expanded rostrally and caudally(Figs. 3C,D, 5A–D, and 6B,D). Rostrally, the maxillareaches nearly as far as the premaxilla and forms mostof the rostrum overlapping the premaxilla in lateralview. The maxilla also forms most of the palate, leavinga long alveolar groove (Alg, Figs. 3C and 5B) laterally tohouse the developing teeth. Tooth buds are not visibleand were probably not mineralized at this stage.

The vomer is ossified at this stage (Vom, Figs. 3D and5A,C); it is a long, narrow bone in the median plane,wedged between the nasal cartilage dorsally, and themaxilla, palatine, and pterygoid bones ventrally. Thevomer does not extend as far rostrally as the maxilla,but it reaches beyond the basisphenoid (Bsp) caudally(Figs. 3D, 5A, and 6A). The nasal bone (Nas) is a smallcircular ossification just medial to the anterior part ofthe frontal and caudal to the external bony nares (Figs.5B and 6B).

The lacrimal (Lac) is a small square bone in the rostralrim of the orbit (Figs. 3C, 5D, and 6D). The lacrimal pro-cess is located at the corner of the lacrimal bone and proj-ects into the orbit. The lacrimal is fused with the jugal(Jug), a needle-shaped bone that extends along the entireventral side of the orbit (Figs. 3C, 5B,D, and 6B,D).

The palatine (Pal) contributes to the caudal section ofthe palate (Figs. 3D, 5A,C, and 6A). At midline, the pala-tine is caudal to the maxilla and rostral to the pterygoid(Ptg, Figs. 3D, 5A,C, and 6A). In the infraorbital region,the palatine forms the lateral wall of the nasal cavity.The pterygoid forms the caudal portion of the palate andforms a hook similar to that in the adult (Mead and For-dyce, 2009).

The frontal bone (Fro) is considerably larger than inthe previous stage and extends medially (Figs. 3C,D,5A,B,D, and 6A,B,D). Rostrally, the frontal bone is over-

lapped by the maxilla (Figs. 3C, 5D, and 6D). The fron-tal bone also forms a distinct supraorbital ridge (Meadand Fordyce, 2009), and this ridge ends as the sharpposterior orbital process (Pop, Figs. 3C, 5B, and 6B,D),which is already developing in these Stenella fetuses.Caudally, the frontal is adjacent to the parietal (Par),but it does not overlap the frontal bone (Figs. 3C,D,5A,B,D, and 6A–D). The parietal is an oval boneand makes up most of the lateral side of the braincase.Ventral to the parietal is the squamosal (Squ, Figs. 3C,5B,C, and 6B,D). The squamosal consists of a pars medi-alis (Prm, Fig. 5D) that will develop into the lateral wallof the braincase, and a pars lateralis (Prl, Fig. 5D) thatwill form the zygomatic process of the squamosal bone.The interparietal bone (Inp) stretches toward the medialplane, making up part of the dorsal roof of the braincase(Figs. 3C,D, 5A,B,D, and 6A–D). There are large fonta-nelles between the interparietal and frontal bones (Figs.5D and 6D) and also between the parietal and supraocci-pital bone (Figs. 5D and 6C).

The dentary (Den) is ossified almost to the rostral tipbut does not reach caudally to the squamosal bone (Figs.3C,D, 5A–D, and 6A,B,D). The dentary, in its rostraltwo-thirds, covers the diminishing Meckel’s cartilagemedially, laterally, and ventrally; it only covers the lat-eral side of Meckel’s cartilage for its caudal third (Figs.3D, 5A, and 6A).

The ectotympanic (Ect) is undergoing ossification(Figs. 3C,D, 5A–C, and 6B). It is horseshoe-shaped andits medial edge is expanding into the ventral middle earwall. This medial edge of the ectotympanic has a rostralprocess. The caudal limb of the ectotympanic terminatesin a semicircular and flat piece of bone. There is no signof a sigmoid process or an involucrum.

Endochondral elements. The chondrocranium isdisappearing at this stage; cartilage is retained mostlyin the ventral midline. The cribriform plate is cartilagi-nous at this stage, but lacks the foramen for CN I pres-ent in the previous stage. The nasal cartilage (Nas crt)or mesorostral cartilage of Mead and Fordyce (2009) islarge and triangular (Fig. 6A). It covers the vomer in themedian plane of Fig. 6, however, the vomer is visible inFigs. 3D and 5A where the skull is cut more laterallyexposing structures lateral to midline. The nasal carti-lage continues caudally to the presphenoid (Pre), whichis a large ossification center present in this area (Figs.3D, 5A, and 6A). The ossification center for the presphe-noid is continuous with that for the orbitosphenoid (Orbsph) in the ala orbitalis (Figs. 3C,D, 5A,B, and 6B). Theventral part of the orbitosphenoid is ossified and theoptic foramen remains large (Opt for, Figs. 3D, 5A,B,and 6B). The dorsal part of the ala orbitalis remains car-tilaginous and is surrounded by the semicircular rim ofthe orbit, as made by the frontal bone.

The ossification center of the basisphenoid (Bsp, Figs.3D, 5A, and 6A) is separated by cartilage from the pre-sphenoid rostrally and is distinct from the basioccipitalbone (Boc) caudally (Fig. 6A). The ala temporalis is pres-ent, but faint and its connections to the ala orbitalis andthe occipital arch are not visible. An oval ossificationcenter for the ali temporalis is present (Alt, Fig. 6B).

Laterally, the exoccipital (Exo) is ossified (Figs. 3C,D,5A,B, and 6B,D) and the rest of the occipital arch is

1752 MORAN ET AL.

cartilaginous and surrounds the foramen magnum.There are clear cartilaginous occipital condyles presentat this stage. Dorsally, the supraoccipital bone (Soc) isossified (Fig. 3C,D, 5A,B,D, and 6A–D). It is a diamond-shaped, bilateral ossification in LACM 94592. In LACM94310, the supraoccipital bone is slightly larger and con-sists of three parts. Right (RSoc, Fig. 6C) and left (LSoc,Fig. 6C) ossifications are bilaterally paired dorsallyand a single ventral ossification is present caudally (Soc,Fig. 6C). The supraoccipital bone stretches from the fo-ramen magnum to where the interparietal and parietalbones meet. The supraoccipital bone does not overlapwith any other bone (Fig. 6C). The supraoccipital is notfused to the interparietal bone at this time. The otic cap-sule is faint and displays no morphological details.

Only the most caudal portion of Meckel’s cartilageremains continuous with the cartilaginous malleus (Mal)of the middle ear (Fig. 4C,D). The manubrium (Man) ofthe malleus is thick and points ventrocaudally. Theaccessory ossicle (Acc, Fig. 4C,D) is a densely ossified,circular structure that overlies, and is fused to, Meckel’scartilage (Mec, Fig. 4C,D). It is not fused to the ectotym-panic as in adult odontocetes (Luo, 1998). The head ofthe malleus is distinct and separate from Meckel’s carti-lage and is located slightly ventral to Meckel’s cartilage(Fig. 4C,D). The incus (Inc, Fig. 3C) is cartilaginous,with the crus longum (Crl, Fig. 4C,D) directed ventrallyand articulating with the faintly visible cartilaginousstapes (Stp, Fig. 4C,D). The crus breve (Crb) points cau-dally (Fig. 4C,D). The crus longum is still more robustthan the crus breve.

The hyoid is connected to the chondrocranium cau-dally. The bar-shaped stylohyoid (Sth) is ossifying and isbetween two cartilaginous sections of the hyoid (Figs.3C,D, 4C,D, 5B, and 6B,D). The distal cartilage bar con-nects to the oval basihyoid cartilage (Bas crt), fromwhich the thyrohyoid cartilage (Thh crt) extends cau-dally (Figs. 5B and 6B). The basihyoid and thyrohyoidare not ossified.

Carnegie Stage 23

Intramembranous elements. The premaxilla(Pmx) and maxilla (Max) are in close contact in thisstage of development and extend rostrally the sameamount (Fig. 7B). Caudally, the premaxilla widensagainst the orbit and forms the lateral edge of the exter-nal bony nares (Ebn, Fig. 7A). The maxilla has a long al-veolar groove (Alg, Fig. 7B), and tooth buds are visiblein the soft tissue of this specimen near this groove. Themaxilla overrides most of the frontal bone (Fro) as wellas the lacrimal bone (Lac) and nearly reaches to theedge of the orbit (Fig. 7B). Medially, the maxilla touchesthe nasal bone. The vomer has a dorsal groove in whichthe nasal cartilage is located. The vomer extends cau-dally as far as the basisphenoid (Bsp, Fig. 7A). The lacri-mal is distinct from, and in contact with, the frontal andmaxilla bones (Lac, Fig. 7B,D).

The palatine (Pal) is separated from the pterygoid(Ptg) by the premaxilla (Pmx, Fig. 7A). The pterygoid iscaudal to the palatine bone and is longer in the rostro-caudal dimension as well as in the dorso-ventral dimen-sion compared to the palatine bone (Fig. 7A). The pala-tine has a limited distribution on the caudal palate,wedged between the maxilla and pterygoid bones. The

pterygoid projects ventrocaudally, as in the adult skull.The pterygoid does not have any visible airsacs at thisstage. No medial or lateral pterygoid plates are present.

The frontal bone is expanded to form most of the ros-tral wall of the braincase (Fro, Fig. 7B,D). Laterally, thefrontal bone forms the dorsal edge of the orbit. The parie-tal (Par) forms the lateral wall of the braincase (Fig. 7B–D). The interparietal (Inp) is large and square-shapedand forms the roof of the braincase (Fig. 7B,C). The fron-tal, parietal, and interparietal bones are separated bynarrowing sutural zones and do not overlap (Fig. 7B).The parietal is overlaid to a small extent by the parsmedialis (Prm) and pars lateralis (Prl) of the squamosal(Squ, Fig. 7B,D). The supraoccipital (Soc) forms a largepart of the caudal wall of the braincase and is not fusedto interparietal or parietal bones (Fig. 7B,C). Both theinterparietal and supraoccipital bones are fused acrossthe midline to their contralateral bone. The fontanelle isnarrower than in the previous stage rostral to the inter-parietal bone adjacent to the frontal bone and betweenthe frontal and parietal bones (Fig. 7A–C).

The jugal bone (Jug) is a narrow, well-ossified bar thatforms most of the ventrolateral edge of the orbit (Fig.7B,D). Rostrally, it is fused firmly with the lacrimal bone(Fig. 7B,D). The pars lateralis (Prl) of the squamosalbone is greatly expanded and nearly touches the jugal(Fig. 7D).

The body of the dentary (Den) is ossified, but the cau-dal and rostral parts of it are not ossified (Fig. 7A,B,D).Caudally, the dentary leaves a large mandibular fora-men through which Meckel’s cartilage emerges. Themandibular condyle is not ossified (Fig. 7D). The man-dibular foramen (Man for), where the acoustic fat pad islocated in adult odontocetes, is visible in Fig. 7A.

The horseshoe-shaped ectotympanic bone is ventral tothe squamosal bone (Ect, Fig. 7B,D). The ventral side of theectotympanic is expanding medially forming the ventralwall of the middle ear cavity, but no involucrum is present.

Endochondral elements. Little remains of thechondrocranium at this stage. The cribriform plate isnot perforated as in the youngest stage. The nasal carti-lage (Nas crt), is thick and triangular, filling the entiremedian plane of the rostrum, and is continuous with themedial portion of the chondrocranium (Fig. 7A). The pre-sphenoid bone (Pre) is firmly fused to the orbitosphenoid(Orb sph, Figs. 7A,B). The optic foramen, which previ-ously perforated the orbitosphenoid, now notches thisbone from the caudal side. The optic foramen is thusfused with the sphenorbital fissure as in the adult(Mead and Fordyce, 2009). The frontal bone extends ven-trally in the wall of the braincase, but wide gaps remainbetween it and the orbitosphenoid. As such, the orbitos-phenoid is surrounded by unossified fontanelles rostrally,dorsally, and caudally.

The ala temporalis (Alt, Fig. 7A,B) is a thick ovalbone, connected by a thin cartilaginous bridge to thebasisphenoid (Bsp, Fig. 7A). The basioccipital (Boc) ismuch larger than the basisphenoid and has a shortflange that is directed ventrolateral (Fig. 7A). This is thefalcate process or basioccipital crest of the adult basiocci-pital bone (Mead and Fordyce, 2009).

The middle ear ossicles and otic capsule are notclearly visible at this stage and are probably close to the

DEVELOPMENT OF THE SKULL OF S. attenuata 1753

stage where they undergo ossification. The accessory os-sicle (Acc) is heavily ossified (Fig. 7D) and remainsattached to an ossified part of Meckel’s cartilage. Theoccipital condyles remain cartilaginous, and so does thedorsal part of the occipital arch adjacent to the foramenmagnum.

The exoccipital (Exo) forms part of the caudal wall ofthe braincase (Fig. 7B). A process from the exoccipitalextends into the hyoid arch. The hyoid arch containsossification centers in the stylohyoid (Sth) and thyro-hyoid (Thh, Fig. 7B,D), but the basihyoid cartilage (Bascrt) is not ossified at this stage.

DISCUSSION

This study allows us to discuss in detail some adapta-tions that are of general interest in the development ofthe skull in S. attenuata from stage 20 to stage 23 ofThewissen and Heyning (2007). These adaptations relateto key cranial anatomical elements of the cetacean skull.Here, we will discuss telescoping of the skull, nasalanatomy, and the development of the middle ear and earanatomy.

Telescoping

Telescoping in odontocetes is defined by the position-ing of the maxilla and premaxilla in the skull (Miller,1923; Kellogg, 1928a, 1928b). The premaxilla and theascending process of the maxilla override the frontal andthe parietal bones pushing dorsally and caudally (Miller,1923; Oelschlager, 1990; Comtesse-Weidner, 2007). Thisdorsal movement of anterior skeletal elements alters thelocation of the sutures between specific bones (Miller,1923). The premaxilla touches the supraoccipital boneand the nasal, premaxilla, maxilla, parietal, and frontalbones are all in close contact (Miller, 1923). The result oftelescoping in odontocetes is the reduction in the inter-temporal region of the skull and it has been suggestedthat this facilitates anatomical adaptations for echoloca-tion (Kellogg, 1928a; Oelschlager, 1990). Telescopingresults in altering the shape of the anterior cranium andflattening of the cranial bones (Reidenberg and Laitman,2008), to form a cradle or basin for the melon (Miller,1923). The initial phase of telescoping during develop-ment can be seen in four (LACM 94592, 94310, 94285,94382) of the five Stenella fetuses presented in thisarticle.

In addition to telescoping, external bony nares posi-tion changes. This is directly and functionally related tothe environment in which these animals live (Miller,1923; Howell, 1930; Klima, 1995; Rommel et al., 2009).The external bony nares moves its position from the tipof the rostrum to the top of the forehead (Klima, 1995;Thewissen et al., 2009). The dorsal movement of theexternal bony nares appears gradually in evolution inprotocetids and basilosaurids and throughout modernwhales (Thewissen et al., 2009). As the premaxilla andmaxilla extend dorsally, the external bony nares ispushed dorsally to the top of the cranium leaving a thinsliver of frontal bone exposed in adult odontocetes(Miller, 1923).

The shifting of cranial bone position is unique to odon-tocete telescoping (Miller, 1923; Kellogg, 1928a). Thisrelative displacement of cranial bones is not present in

Eocene whales or mysticetes (Miller, 1923; Kellogg,1928a) The mysticete maxilla cannot override the frontalbone due to its two bony processes (Kellogg, 1928a). Theascending process of the maxilla overlaps the frontalbone while the infraorbital process of the maxilla liesunder the frontal bone securing the maxilla in position(Kellogg, 1928a). Rostral movement of cranial bonesoccurs in mysticetes with the posteriorly located occipitalbone pushing rostrally (Kellogg, 1928b). This rostralshift in mysticetes is also called telescoping (Miller,1923).

In S. attenuata, the maxilla does not override the fron-tal and parietal bones in the early stage 20 fetus (Figs.2A,B and 3A,B), but the later fetuses do show evidenceof telescoping (Figs. 3C,D and 5–7). Specifically, the latestage 20 (LACM 94592, Fig. 5) and the stage 21/22(LACM 94310, Fig. 6) fetuses exhibit the beginning oftelescoping (Figs. 3C, 5D,and 6D). The premaxilla iselongated rostrally in LACM 94592 (Figs. 3 and 5). Themaxilla reaches dorsally as far as the middle of theorbit. The maxilla and the premaxilla are located dor-sally and partly overlap the parietal and frontal bones(Figs. 3C,D, 5A,B, and 6A,B). In stage 21/22, the gapbetween the frontal bone and the maxilla is not visible(Figs. 5D and 6D). Even less of the frontal bone isexposed in the older fetuses (LACM 94285 and 94382,stage 23) as telescoping is well underway.

Nasal Anatomy

The nasal anatomy of cetaceans is unique amongmammals (Klima, 1995). The median nasal cartilage, aswell as the bony elements of the rostrum, acts as a con-duit for echolocation emissions (Cranford et al., 1996;Klima, 1999). Klima (1999) suggested the median nasalcartilage aids the growth of the embryonic rostrum inlength before the bony elements are in place. Histologi-cally, the median nasal cartilage is different from thecartilaginous nasal septa of land mammals due to thehigh amount of fibrous cartilage and interwoven fiberbundles (Klima, 1999).

The vomer is a thin triangular wedge of bone in thepalate of LACM 94592 (Fisg. 3D and 5A,C). The vomeris rostrally almost as long as the maxilla and flares dor-soventrally near the inferior edge of the orbit (Fig. 5A).The vomer provides a cradle (the mesorostral furrow),along with the paired premaxillae, for the median nasalcartilage. The vomer grows in length as the maxilla andpremaxilla lengthen and the rostrum elongates.

The median nasal cartilage has the shape of an equi-lateral triangle and is one of the most conspicuous partsof the dolphin skull in the early stage 20 fetus, LACM94671 (Figs. 2A and 3B). The median nasal cartilageflares dorsally and is elongated with the outgrowth ofthe rostrum in late stage 20 and stages 21/22. Thislengthening can be seen in LACM 94310 (Fig. 6A). Themedian nasal cartilage is continuous with the chondroc-ranium (Fig. 6A). The median nasal cartilage does notcompletely reach to the rostral tip as the premaxillarycartilage is still present at the very tip of the rostrumeven at stage 23 of development (Fig. 7A,B). There isminor change in the median nasal cartilage after latestage 20. The monkey lip dorsal bursae or phonic lips(Au, 1993; Cranford et al., 1996; Berta et al., 2006) arenot visible in any of the fetal stages discussed here.

1754 MORAN ET AL.

Ear Anatomy

The three middle ear ossicles (the malleus, incus, andstapes) transmit sound from the tympanic membrane tothe inner ear (Williams et al., 1995). Lancaster (1990)made theoretical predictions of the position of the middleear ossicles in transitional cetacean ears based on thefossil record. Thewissen and Hussain (1993), Thewissenet al. (2009), and Nummela et al. (2004, 2006) docu-mented transitional morphologies in fossils such as paki-cetids, remingtonocetids, protocetids, and basilosaurids.

Sound transmission characteristics differ between airand water prompting evolutionary change in the anat-omy and morphology of the middle ear of cetaceans(Nummela et al., 2007). Fifty million years ago, pakice-tids had middle ear anatomy that was more similar toland mammals than modern cetaceans (Nummela et al.,2004). Pakicetids have a small mandibular foramen andlacked a mandibular fat pad, suggesting that these earlywhales did not hear well in water (Thewissen and Hus-sain, 1993; Nummela et al., 2007). Ambulocetus, reming-tonocetids, and protocetids have a large mandibularforamen and, where known, middle ear ossicles thatmorphologically are more similar to modern cetaceans(Nummela et al., 2004, 2007). The 35 million year oldmiddle ear of basilosaurids is considered fully modern(Nummela et al., 2004).

Echolocating cetaceans have a pachyosteosclerotictympanoperiotic complex that is isolated from the skullby air-filled sinuses (Purves, 1966; Oelschlager, 1990;Nummela et al., 2007; Cranford et al., 2010; Hemilaet al., 2010). This isolation of the ear from the skullallows for directional hearing in water and the sinuseschange volume during pressure changes when diving(Oelschlager, 1990; Reidenberg and Laitman, 2008). Theisolation of the tympanoperiotic complex in archaeocetesthrough modern cetaceans provides more movement ofthe tympanic plate. This relays sound from the water,through the mandible, to the middle ear ossicles forhearing (Fleischer, 1978; Luo, 1998; Nummela et al.,2007; Cranford et al., 2010; Hemila et al., 2010). Isola-tion of the tympanoperiotic complex is not definitivelyexhibited in the Stenella fetuses.

The involucrum is the thickened medial wall of thetympanic bone in adults; the lateral wall is thin enoughto see light shine through (Nummela et al., 2007). Thismorphology is present in the earliest whales, back topakicetids, and is characteristic of cetacean ears (Num-mela et al., 2007; Thewissen et al., 2009). The smalltympanic ring is a U-shaped ridge of bone located on thethin lateral wall of the tympanic bone. It is where thetympanic ligament attaches (Oelschlager, 1990). None ofour five embryos have an involucrum and the tympanicring is not visible. The pharyngotympanic tube is notvisible in any of the fetal stages discussed here.

The middle ear ossicles of cetaceans form a chainwithin the tympanic bone, as in land mammals, but theorientation of the ossicles is different (Nummela et al.,2007; Cranford et al., 2010). Fleischer (1973, 1976, 1978)noted the unusual position of the auditory ossicles incetaceans. The manubrium of the malleus is reduced inlength (Fraser and Purves, 1960; Purves, 1966; Oelschl-ager, 1990) and points ventrally extending in a parasag-ittal plane in land mammals. The cetacean incus isorientated so the crus breve and crus longum are rotated

and point medially (Fleischer, 1978; Oelschlager, 1990;Kinkel et al., 2001). Kinkel et al. (2001) described theembryology of S. attenuata ossicles based on histologicalsections of specimens. The cetacean malleus and incuswere found to be rotated approximately 90 degreesaround the physiological axis of rotation (Thewissen,1994; Kinkel et al., 2001). This is considerably more rota-tion than seen in Pakicetus, which is considered to be theintermediate between land mammal ossicle orientationand cetacean orientation (Thewissen and Hussain, 1993).

The rotation of the middle ear ossicles can be seen in Fig.4. The crus longum (Crl) of the incus has started to turnmedially and elongate in LACM 94592 (Fig. 4C,D) exposingthe stapes. The malleus is also continuing to develop andseparate from Meckel’s cartilage in Fig. 4C and D.

The accessory ossicle is a middle ear structure dis-tinct, but synostosed in mysticetes and odontocetes, aswell as some fetal artiodactyls (Luo, 1998; Mead andFordyce, 2009). The accessory ossicle is homologous withthe embryonic accessory ossicle in artiodactyls, whichdevelops into the processus tubarius and merges intothe bulla (Oelschlager, 1990; Luo, 1998). Embryonicallyin odontocetes, the accessory ossicle changes in onlyminor ways from its fetal shape (Fig. 4) to the adultshape (Luo, 1998). The adult odontocete accessory ossicleis actually more similar to a fetal mysticete accessory os-sicle (Luo, 1998). In adult mysticetes, the accessory ossi-cle fuses with the anterior process of the petrosalforming a gracile pedicle connecting but not synostosingwith the bulla or processus tubarius (Luo, 1998). Theaccessory ossicle provides an anterior junction betweenthe tympanic bone and the periotic bone (Oelschlager,1990) and is visible just rostral to the malleus in LACM94592 (Fig. 4C,D). The function of this structure is notpart of the middle ear model as outlined by Nummelaet al. (2004, 2007) or Cranford et al. (2010).

CONCLUSION

Cleared and stained specimens provide a greatresource for studying morphological developmentalchanges in vertebrates. Direct interpretation of anatomyfrom bony and cartilaginous structures is imperative forontogenetic comparisons. Cleared and stained specimensare more easily interpreted than serial histological sec-tions and allow for morphological comparisons to fossils.These morphological studies can help guide moleculartechniques, such as immunohistochemistry and in situhybridization, in understanding the protein and mRNAexpression in cartilage and bone.

ACKNOWLEDGEMENTS

We would like to thank Sharon Usip for all her helpin the lab and in the staining process.

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