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Development of the Skull of the Pantropical Spotted Dolphin (Stenella attenuata).

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THE ANATOMICAL RECORD 294:1743–1756 (2011)
Development of the Skull of the
Pantropical Spotted Dolphin (Stenella
attenuata)
1
MEGHAN M. MORAN,1* SIRPA NUMMELA,2 AND J.G.M. THEWISSEN1
Department of Anatomy and Neurobiology, Northeastern Ohio Universities Colleges of
Medicine and Pharmacy, Rootstown, Ohio
2
Department of Biosciences, University of Helsinki, Helsinki, Finland
ABSTRACT
We describe the bony and cartilaginous structures of five fetal skulls
of Stenella attenuata (pantropical spotted dolphin) specimens. The specimens represent early fetal life as suggested by the presence of rostral tactile hairs and the beginnings of skin pigmentation. These specimens
exhibit the developmental order of ossification of the intramembranous
and endochondral elements of the cranium as well as the functional and
morphological development of specific cetacean anatomical adaptations.
Detailed observations are presented on telescoping, nasal anatomy, and
middle ear anatomy. The development of the middle ear ossicles, ectotympanic bone, and median nasal cartilage is of interest because in the adult
these structures are morphologically different from those in land mammals. We follow specific cetacean morphological characteristics through
fetal development to provide insight into the form and function of the
cetacean body plan. Combining these data with fossil evidence, it is possible to overlie ontogenetic patterns and discern evolutionary patterns of
C 2011 Wiley-Liss, Inc.
the cetacean skull. Anat Rec, 294:1743–1756, 2011. V
Key words: cranial development; Stenella attenuata; telescoping;
middle ear; Cetacea
The development of the Cetacea skull was studied in
embryos (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). Cetacean
research focused on specific biological systems to understand differences within Mammalia. Comtesse-Weidner
(2007), Miller (1923) and Kellogg (1928a, 1928b) studied
morphological elements including telescoping. Oelschläger and Buhl (1985), Klima and van Bree (1990), and
Klima (1995, 1999) studied nasal anatomy and development. Oelschläger (1986, 1990), Solntseva (1990, 1999,
2002), and Kinkel et al. (2001) concentrated on hearing
reception and sound emission while Mead and Fordyce
(2009) focused on general skull anatomy. Although comparative embryological studies on cetaceans were rare,
developmental studies were mostly nonexistent. Such
studies (e.g., Thewissen et al., 2006, Armfield et al., in
press) allow for a deeper understanding of the ontogenetic constraints on the evolution of the cetacean body
plan.
C 2011 WILEY-LISS, INC.
V
Habitat changes alter adaptations for specific cetacean
body plans. These modifications include those of anatomical function and body plan from land mammals to fully
aquatic, air breathing marine mammals. Our study
focuses on anatomical structures of five Stenella attenuata (pantropical spotted dolphin) fetuses. Here we
describe 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 Anatomy and Neurobiology, 4209 State Route 44, P.O. Box 95,
Northeastern Ohio Universities Colleges of Medicine and Pharmacy, 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.21388
Published online 8 September 2011 in Wiley Online Library
(wileyonlinelibrary.com).
1744
MORAN ET AL.
Fig. 1. Five cleared and stained pantropical spotted dolphin (Stenella attenuata) fetuses. Alcian blue
stains the cartilage and Alizarin red stains the bone. Specimen numbers are listed to the left of each fetus. LACM 94671 is early stage 20, TL: 85 mm. LACM 94592 is late stage 20, TL: 155 mm. LACM 94310
is stage 21/22, TL: 185 mm. LACM 94285 is stage 23, TL: 213 mm. LACM 94382 is stage 23, TL: 225
mm. Scale bar ¼ 1 cm.
TABLE 1. Stenella attenuata fetal specimen details
Specimen number
94671
94592
94310
94285
94382
Stage
Approximate age
Total length (TL)
Skull length
C20
C20
C21/22
C23
C23
70 days
80–110 days
80–110 days
110–120 days
110–120 days
85
155
185
213
225
20
37
45
56
58
Specimen numbers, expanded Carnegie stage, associated ages, as well as average body length and average skull length in
millimeters (based on Stěrba et al., 2000).
DEVELOPMENT OF THE SKULL OF S. attenuata
cranium of these fetuses to elucidate telescoping, nasal
anatomy, and ear anatomy.
1745
in Figs. 1 and 6; LACM 94285 in Figs. 1 and 7; and
LACM 94382 in Fig. 1.
MATERIALS AND METHODS
We describe the skulls of five S. attenuata fetuses
from the Natural History Museum of Los Angeles
County (LACM) in Los Angeles, CA (Fig. 1). These
fetuses are staged using the adapted and expanded
Carnegie system from Thewissen and Heyning (2007).
Ages of fetuses are based on Štěrba et al. (2000).
The five specimens are: LACM 94671, LACM 94592,
LACM 94310, LACM 94285, and LACM 94382 (Fig. 1
and Table 1).
Each fetus is measured by placing a piece of string
along the dorsum of the fetus from the rostral tip to the
tail 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 of
the occipital bones and cartilage. Each measurement is
taken three times and the average is listed in this table.
No linear measurements of individual bones are presented because the vast shape change of cranial bones
during development makes it difficult to take measurements consistently.
Each Stenella fetus is cleared and stained (Wassersug,
1976) to show only bone and cartilage structures. Other
soft tissue structures are obliterated during the staining
process. The specimen is skinned, eviscerated, and
washed in water for about 7 days to remove fixative.
The head is bisected to allow for better visualization of
the cranial bones and cartilaginous areas after staining.
This also allows for further molecular study to be completed on the contralateral side of each fetal skull specimen. Symmetry was not addressed during cranial
development because this technique made it impossible.
The water is changed every day to maximize the washing process. The fetus is then put into a 40% acetic acid/
60% alcohol solution for 7 days. Again, the solution is
changed every day. After 7 days in the 40% acetic acid/
60% alcohol solution, the solution is replaced and Alcian
blue stain is added to the solution. The Alcian blue
stain/acetic acid/alcohol solution is checked every day;
the solution is replaced every 23 days for anywhere
between 5 days to 4 weeks depending on how well the
specimen absorbs the stain. The Alcian blue stains the
cartilaginous structures of the specimen.
Once the blue stain is absorbed by the cartilage, the
specimen is placed in a 3–5% potassium hydroxide/Alizarin red stain solution for 1 day or until the bone absorbs
the red stain. This solution is checked every hour to prevent any damage the specimen because this solution is
extremely caustic and tissue quickly deteriorates. The
Alizarin red stains the bone red. The double stained dolphin fetus is placed into a series of rinses of increasing
concentrations of glycerol from 25% to 100%. Each fetus
is stored in 100% glycerol in the refrigerator (4 C).
Slight differences in the timing of these steps may occur
because 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
Early Carnegie Stage 20
Intramembranous elements. The premaxilla
(Pmx) is an elongated bone, constricted to a narrow
waist near its middle (Figs. 2A,D and 3A,B). The left
and right premaxillae (Fig. 2A and D) are wedged
between the left and right maxillae (Max, Figs. 2B,D
and 3A,B) and do not extend into the rostrum. The rostrum lacks much ossification at this time. The premaxilla reaches farther rostrally than the maxilla. A small
and dense piece of premaxillary cartilage (Pmx crt) is
located at the tip of the rostrum (Figs. 2A,B and 3A,B).
The external bony nares (Ebn, Fig. 2A) is caudal to the
premaxilla, high on the forehead. Medial to the premaxilla, a number of cartilaginous structures are associated
with the nasal cartilage and vomer. The development of
these structures has been described in some detail by
Klima (1999) and will not be discussed here.
The maxilla (Figs. 2B,D and 3A,B) is a triangular
bone on the lateral side of the face and forms a narrow
portion of the palate. The maxilla forms most of the rostrum at this stage. The caudal aspect of the maxilla is
located lateral to the cribriform plate (Cbp, Figs. 2A and
3B) and the nasal cartilages. The maxilla extends dorsally but not as far as the frontal (Fro) and parietal
(Par) bones (Figs. 2B and 3A). Medially, the maxilla is
gently concave and helps support the well-developed median nasal cartilage (Nas crt, Figs. 2A and 3B) or mesorostral cartilage (see Mead and Fordyce, 2009).
Posterior to the maxilla, the lacrimal (Lac, Figs. 2D
and 3A) is a narrow splint of bone in the anterior edge
of the orbit. In the wall of the pharynx, two ossification
centers are posterior to the maxilla. The more anterior
of the two ossifications is the palatine (Pal, Figs. 2A and
3B), which makes up the lateral wall of the nasopharyngeal duct. Caudal to the palatine is the pterygoid bone
(Ptg, Figs. 2A and 3B), which extends more ventrally
than the palatine. The vomer (Vom) is located medially
to the palatine and the pterygoid (Fig. 3B).
The frontal bone (Figs. 2B,D,E and 3A,B) is a flat, rectangular bone that forms the ventrally concave edge of
the dorsal orbit. The frontal bone does not extend into
the roof of the orbit and does not overlap with any other
bones in this specimen (Figs. 2B and 3A). The parietal
bone (Par, Figs. 2B,D and 3A) is a flat, teardrop-shaped
bone immediately caudal to the frontal bone and dorsal
to the otic capsule (Otc, Figs. 2A,B,E and 3A). The squamosal bone (Squ, Figs. 2B,D and 3A) is a small bone
located over the posterior end of Meckel’s cartilage, adjacent to the otic capsule (Mec, Figs. 2A,B,D and 3A,B).
The dentary at this stage is ossified from the ramus
through the central part of the dentary (Den, Figs.
2A,B,D and 3A,B). This ossification starts at the anterior
edge of Meckel’s cartilage near the tip of the rostrum
and ends near the middle of the orbit. The dentary is
concave medially, enveloping Meckel’s cartilage and
wrapping around it ventrolaterally. The ectotympanic
(Ect) is a very thin horseshoe-shaped ossification located
ventral to the squamosal bone (Fig. 2D) and inferior to
the posterior end of Meckel’s cartilage.
Fig. 2. Head of fetus LACM 94671 (TL: 85 mm), A: median. B: lateral. C: before clearing and staining; the soft tissue structures are in
situ such as the brain, epiglottis, and the tongue. D: Close up of the
cranium from an inferior–lateral orientation. E: Superior–medial view of
the median cranial structures. Specific cartilaginous and bony features
are labeled in the figure. Scale bar ¼ 5 mm for A–C and E. Scale does
not apply to D which is foreshortened. Abbreviations in Figs. 2–7: Acc,
accessory ossicle; Alg, alveolar groove; Alo, ala orbitalis; Alt, Ala temporalis; Bas crt, basihyoid cartilage; Boc, basioccipital bone; Boc crt,
basioccipital cartilage; Bsp, basisphenoid bone; Bsp crt, basisphenoid
cartilage; Cbp, cribriform plate; Crb, crus breve of the incus; Crl, crus
longum 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, jugular
foramen; Jug, jugal bone; Lac, lacrimal bone; LSoc, left ossification of
the 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, presphenoid
bone; Pre crt, presphenoid cartilage; Prl, pars lateralis of the squamosal
bone; Prm, pars medialis of the squamosal bone; Ptg, pterygoid bone;
RSoc, right ossification of the supraoccipital bone; Soc, supraoccipital
bone; Sph fis, sphenorbital fissure; Squ, squamosal bone; Sth, stylohyoid bone; Sth crt, stylohyoid cartilage; Stp, stapes; Thh, thyrohyoid
bone; Thh crt, thyrohyoid cartilage; Ton, tongue; Vom, vomer bone.
DEVELOPMENT OF THE SKULL OF S. attenuata
1747
Fig. 3. Comprehensive black and white line drawings of the developing skulls of LACM 94671. A: Lateral, and B: medial views. LACM 94592, C: lateral and D: medial views. Some structures drawn here are
not represented in the photographs but were observed through the microscope. The course stipples represent cartilage and the fine stipples represent bone.
Endochondral elements. The nasal capsule forms
the rostral wall of the cranial cavity. The cribriform
plate is perforated by a large bilateral foramina for cranial nerve I (CN I) immediately lateral to the midline.
Projecting rostrally in the midline is the large median
nasal cartilage (Nas crt, Figs. 2A and 3B), rostrum nasi
cartilagineum of Klima (1995, 1999). The lateral wall of
the nasal capsule is barely developed, consisting only of
a few isolated pieces of cartilage. The ethmoid is
bounded caudally by the large orbitonasal fissure (Orb
fis, Figs. 2A,B and 3B). Dorsal to the orbitonasal fissure,
a thin cartilaginous process connects the nasal capsule
to the ala orbitalis (Alo, Figs. 2A,B,E and 3B). Such a
process is not present in a 48 mm Phocoena (de Beer,
1748
MORAN ET AL.
Fig. 4. Close up views of the middle ear structures including ossicles. A: LACM 94671, B: black and
white 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.
1937) but is present in a 92 mm Megaptera (Honigmann,
1917). The ala orbitalis appears as a cartilaginous ring
and is perforated by the optic foramen (Opt for, Figs.
2A,B,E and 3A,B). This foramen is laterally placed and
large as in the 48 mm Phocoena (de Beer, 1937), unlike
the 92 mm Megaptera (Honigmann, 1917). Caudally, the
ala 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 far
dorso-laterally to make up the lateral wall of the
braincase.
The median bones of the chondrocranium are not ossified at this stage. The presphenoid cartilage (Pre crt,
Figs. 2A and 3B) is thick, short, and fused along its
entire length with the ala orbitalis. The basisphenoid
cartilage (Bsp crt, Figs. 2A and 3B) is thinner dorsoven-
trally and longer than the presphenoid cartilage. It is
continuous with the basioccipital cartilage (Boc crt, Figs.
2A and 3B). The median cartilages can also be seen in
the median view of the head before any staining was
completed (Fig. 2C).
Dorsal to the foramen magnum is the supraoccipital bone (Soc, Figs. 2A,B and 3A,B). The supraoccipital bone is a small kidney-shaped ossification of
the chondrocranium at the most posterior portion of
the skull. The supraoccipital, exoccipital, and basioccipital are not ossified, but their cartilaginous precursors form a complete caudal wall to the cranial
cavity.
The otic capsule is large and reaches nearly to the
midline (Otc, Figs. 2A,B,E and 3A). On the endocranial
side, it has a separate foramen (internal auditory
DEVELOPMENT OF THE SKULL OF S. attenuata
1749
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.
meatus) for the facial and statoacoustic nerves. The internal auditory meatus (Iam, Fig. 2E), and the large basal whorl of the cochlea can be seen inside the otic
capsule. A small foramen pierces the otic capsule laterally, and may represent the endolymphatic duct (End
for, Fig. 2E), as previously identified by de Beer (1937)
in Phocoena. The occipital arch, the cartilaginous precursor to the exoccipital and basioccipital bones, makes up
the caudal part of the chondrocranium. The occipital
arch extends far dorsally and connects to the ala
1750
MORAN ET AL.
Fig. 6. The head of LACM 94310 (TL: 185 mm). A: Medial, B: Lateral, C: Dorsal, D: Superior–lateral
orientation. Scale bar ¼ 1 cm for A–D.
temporalis in the lateral wall of the braincase. A large
occipitocapsular fissure (de Beer, 1937) is located superior to the otic capsule and ventral to the supraoccipital
bone separating the ala temporalis and the occipital
arch (Occ fis, Fig. 2A,E). The large, slit-like jugular
foramen (Jfr, Fig. 2E) separates the otic capsule from
the occipital arch. Immediately caudal to the jugular
foramen is the hypoglossal canal (Hyp, Fig. 2E), and
immediately medial to the jugular foramen is a small
foramen, possibly for the ventral petrosal sinus.
DEVELOPMENT OF THE SKULL OF S. attenuata
1751
Fig. 7. The head of LACM 94285 (TL: 213 mm). A: Median. B: Lateral. C: Dorsal. D: Inferior–lateral
orientation. Scale bar ¼ 1 cm for A–C. Scale bar ¼ 2 cm for D.
The middle ear ossicles are located caudal to Meckel’s
cartilage (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 the
incus points ventrally, and the crus breve (Crb) points
caudally (Fig. 4A,B). The crus longum is slightly thicker
than the crus breve. The stapes is faintly visible oriented
mediolaterally between the crus longum and otic capsule.
1752
MORAN ET AL.
Meckel’s cartilage (Mec) is a solid structure surrounded by the dentary (Figs. 2A,B,D, 3A,B, and 4A,B).
Meckel’s cartilage projects rostrally and ventrally to the
squamosal bone (Fig. 2B). Near its rostral extremity, the
cartilage fades where it is in close contact with the ossifying dentary.
The stylohyoid (Sth crt) and the thyrohyoid (Thh crt)
cartilages are two bars of cartilage ventral to Meckel’s
cartilage (Figs. 2B,D, 3A,B, and 4A,B). The stylohyoid
projects as a straight cartilage bar from the chondrocranium. Ventrally, the stylohyoid cartilage is connected to
the basihyoid cartilage, which was damaged during
preparation of this specimen. The thyrohyoid is a narrow
bar of cartilage that projects caudally from this area toward the laryngeal cartilages. No ossification centers are
present 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 rostrum
but does not reach into the tip as a small remnant of the
premaxillary cartilage remains (Pmx crt, Figs. 5B and
6A,B,D). Caudally, the dorsal aspect of the premaxilla is
perforated by a foramen, presumably for a branch of the
infraorbital nerve and its associated vessels. Caudally
the premaxilla ends in a narrow process, rostral to the
external bony nares (Ebn, Figs. 5A and 6A). The premaxilla is not fused to the maxilla but these two bones
are adjacent to each other.
The maxilla (Max) is expanded rostrally and caudally
(Figs. 3C,D, 5A–D, and 6B,D). Rostrally, the maxilla
reaches nearly as far as the premaxilla and forms most
of the rostrum overlapping the premaxilla in lateral
view. The maxilla also forms most of the palate, leaving
a long alveolar groove (Alg, Figs. 3C and 5B) laterally to
house the developing teeth. Tooth buds are not visible
and were probably not mineralized at this stage.
The vomer is ossified at this stage (Vom, Figs. 3D and
5A,C); it is a long, narrow bone in the median plane,
wedged between the nasal cartilage dorsally, and the
maxilla, palatine, and pterygoid bones ventrally. The
vomer 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 small
circular ossification just medial to the anterior part of
the frontal and caudal to the external bony nares (Figs.
5B and 6B).
The lacrimal (Lac) is a small square bone in the rostral
rim of the orbit (Figs. 3C, 5D, and 6D). The lacrimal process is located at the corner of the lacrimal bone and projects into the orbit. The lacrimal is fused with the jugal
(Jug), a needle-shaped bone that extends along the entire
ventral side of the orbit (Figs. 3C, 5B,D, and 6B,D).
The palatine (Pal) contributes to the caudal section of
the palate (Figs. 3D, 5A,C, and 6A). At midline, the palatine 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 and
forms a hook similar to that in the adult (Mead and Fordyce, 2009).
The frontal bone (Fro) is considerably larger than in
the 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 frontal bone also forms a distinct supraorbital ridge (Mead
and Fordyce, 2009), and this ridge ends as the sharp
posterior 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 bone
and 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 medialis (Prm, Fig. 5D) that will develop into the lateral wall
of the braincase, and a pars lateralis (Prl, Fig. 5D) that
will form the zygomatic process of the squamosal bone.
The interparietal bone (Inp) stretches toward the medial
plane, making up part of the dorsal roof of the braincase
(Figs. 3C,D, 5A,B,D, and 6A–D). There are large fontanelles between the interparietal and frontal bones (Figs.
5D and 6D) and also between the parietal and supraoccipital bone (Figs. 5D and 6C).
The dentary (Den) is ossified almost to the rostral tip
but does not reach caudally to the squamosal bone (Figs.
3C,D, 5A–D, and 6A,B,D). The dentary, in its rostral
two-thirds, covers the diminishing Meckel’s cartilage
medially, laterally, and ventrally; it only covers the lateral 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 and
its medial edge is expanding into the ventral middle ear
wall. This medial edge of the ectotympanic has a rostral
process. The caudal limb of the ectotympanic terminates
in a semicircular and flat piece of bone. There is no sign
of a sigmoid process or an involucrum.
Endochondral elements. The chondrocranium is
disappearing at this stage; cartilage is retained mostly
in the ventral midline. The cribriform plate is cartilaginous at this stage, but lacks the foramen for CN I present in the previous stage. The nasal cartilage (Nas crt)
or mesorostral cartilage of Mead and Fordyce (2009) is
large and triangular (Fig. 6A). It covers the vomer in the
median plane of Fig. 6, however, the vomer is visible in
Figs. 3D and 5A where the skull is cut more laterally
exposing structures lateral to midline. The nasal cartilage continues caudally to the presphenoid (Pre), which
is a large ossification center present in this area (Figs.
3D, 5A, and 6A). The ossification center for the presphenoid is continuous with that for the orbitosphenoid (Orb
sph) in the ala orbitalis (Figs. 3C,D, 5A,B, and 6B). The
ventral part of the orbitosphenoid is ossified and the
optic foramen remains large (Opt for, Figs. 3D, 5A,B,
and 6B). The dorsal part of the ala orbitalis remains cartilaginous and is surrounded by the semicircular rim of
the 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 presphenoid rostrally and is distinct from the basioccipital
bone (Boc) caudally (Fig. 6A). The ala temporalis is present, but faint and its connections to the ala orbitalis and
the occipital arch are not visible. An oval ossification
center 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
DEVELOPMENT OF THE SKULL OF S. attenuata
cartilaginous and surrounds the foramen magnum.
There are clear cartilaginous occipital condyles present
at this stage. Dorsally, the supraoccipital bone (Soc) is
ossified (Fig. 3C,D, 5A,B,D, and 6A–D). It is a diamondshaped, bilateral ossification in LACM 94592. In LACM
94310, the supraoccipital bone is slightly larger and consists of three parts. Right (RSoc, Fig. 6C) and left (LSoc,
Fig. 6C) ossifications are bilaterally paired dorsally
and a single ventral ossification is present caudally (Soc,
Fig. 6C). The supraoccipital bone stretches from the foramen magnum to where the interparietal and parietal
bones meet. The supraoccipital bone does not overlap
with any other bone (Fig. 6C). The supraoccipital is not
fused to the interparietal bone at this time. The otic capsule is faint and displays no morphological details.
Only the most caudal portion of Meckel’s cartilage
remains continuous with the cartilaginous malleus (Mal)
of the middle ear (Fig. 4C,D). The manubrium (Man) of
the malleus is thick and points ventrocaudally. The
accessory ossicle (Acc, Fig. 4C,D) is a densely ossified,
circular structure that overlies, and is fused to, Meckel’s
cartilage (Mec, Fig. 4C,D). It is not fused to the ectotympanic as in adult odontocetes (Luo, 1998). The head of
the malleus is distinct and separate from Meckel’s cartilage 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 ventrally
and articulating with the faintly visible cartilaginous
stapes (Stp, Fig. 4C,D). The crus breve (Crb) points caudally (Fig. 4C,D). The crus longum is still more robust
than the crus breve.
The hyoid is connected to the chondrocranium caudally. The bar-shaped stylohyoid (Sth) is ossifying and is
between two cartilaginous sections of the hyoid (Figs.
3C,D, 4C,D, 5B, and 6B,D). The distal cartilage bar connects to the oval basihyoid cartilage (Bas crt), from
which the thyrohyoid cartilage (Thh crt) extends caudally (Figs. 5B and 6B). The basihyoid and thyrohyoid
are not ossified.
Carnegie Stage 23
Intramembranous elements. The premaxilla
(Pmx) and maxilla (Max) are in close contact in this
stage of development and extend rostrally the same
amount (Fig. 7B). Caudally, the premaxilla widens
against the orbit and forms the lateral edge of the external bony nares (Ebn, Fig. 7A). The maxilla has a long alveolar groove (Alg, Fig. 7B), and tooth buds are visible
in the soft tissue of this specimen near this groove. The
maxilla overrides most of the frontal bone (Fro) as well
as the lacrimal bone (Lac) and nearly reaches to the
edge of the orbit (Fig. 7B). Medially, the maxilla touches
the nasal bone. The vomer has a dorsal groove in which
the nasal cartilage is located. The vomer extends caudally as far as the basisphenoid (Bsp, Fig. 7A). The lacrimal is distinct from, and in contact with, the frontal and
maxilla bones (Lac, Fig. 7B,D).
The palatine (Pal) is separated from the pterygoid
(Ptg) by the premaxilla (Pmx, Fig. 7A). The pterygoid is
caudal to the palatine bone and is longer in the rostrocaudal dimension as well as in the dorso-ventral dimension compared to the palatine bone (Fig. 7A). The palatine has a limited distribution on the caudal palate,
wedged between the maxilla and pterygoid bones. The
1753
pterygoid projects ventrocaudally, as in the adult skull.
The pterygoid does not have any visible airsacs at this
stage. No medial or lateral pterygoid plates are present.
The frontal bone is expanded to form most of the rostral wall of the braincase (Fro, Fig. 7B,D). Laterally, the
frontal bone forms the dorsal edge of the orbit. The parietal (Par) forms the lateral wall of the braincase (Fig. 7B–
D). The interparietal (Inp) is large and square-shaped
and forms the roof of the braincase (Fig. 7B,C). The frontal, parietal, and interparietal bones are separated by
narrowing sutural zones and do not overlap (Fig. 7B).
The parietal is overlaid to a small extent by the pars
medialis (Prm) and pars lateralis (Prl) of the squamosal
(Squ, Fig. 7B,D). The supraoccipital (Soc) forms a large
part of the caudal wall of the braincase and is not fused
to interparietal or parietal bones (Fig. 7B,C). Both the
interparietal and supraoccipital bones are fused across
the midline to their contralateral bone. The fontanelle is
narrower than in the previous stage rostral to the interparietal bone adjacent to the frontal bone and between
the frontal and parietal bones (Fig. 7A–C).
The jugal bone (Jug) is a narrow, well-ossified bar that
forms 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 squamosal
bone is greatly expanded and nearly touches the jugal
(Fig. 7D).
The body of the dentary (Den) is ossified, but the caudal and rostral parts of it are not ossified (Fig. 7A,B,D).
Caudally, the dentary leaves a large mandibular foramen through which Meckel’s cartilage emerges. The
mandibular condyle is not ossified (Fig. 7D). The mandibular foramen (Man for), where the acoustic fat pad is
located in adult odontocetes, is visible in Fig. 7A.
The horseshoe-shaped ectotympanic bone is ventral to
the squamosal bone (Ect, Fig. 7B,D). The ventral side of the
ectotympanic is expanding medially forming the ventral
wall of the middle ear cavity, but no involucrum is present.
Endochondral elements. Little remains of the
chondrocranium at this stage. The cribriform plate is
not perforated as in the youngest stage. The nasal cartilage (Nas crt), is thick and triangular, filling the entire
median plane of the rostrum, and is continuous with the
medial portion of the chondrocranium (Fig. 7A). The presphenoid bone (Pre) is firmly fused to the orbitosphenoid
(Orb sph, Figs. 7A,B). The optic foramen, which previously perforated the orbitosphenoid, now notches this
bone from the caudal side. The optic foramen is thus
fused with the sphenorbital fissure as in the adult
(Mead and Fordyce, 2009). The frontal bone extends ventrally in the wall of the braincase, but wide gaps remain
between it and the orbitosphenoid. As such, the orbitosphenoid is surrounded by unossified fontanelles rostrally,
dorsally, and caudally.
The ala temporalis (Alt, Fig. 7A,B) is a thick oval
bone, connected by a thin cartilaginous bridge to the
basisphenoid (Bsp, Fig. 7A). The basioccipital (Boc) is
much larger than the basisphenoid and has a short
flange that is directed ventrolateral (Fig. 7A). This is the
falcate process or basioccipital crest of the adult basioccipital bone (Mead and Fordyce, 2009).
The middle ear ossicles and otic capsule are not
clearly visible at this stage and are probably close to the
1754
MORAN ET AL.
stage where they undergo ossification. The accessory ossicle (Acc) is heavily ossified (Fig. 7D) and remains
attached to an ossified part of Meckel’s cartilage. The
occipital condyles remain cartilaginous, and so does the
dorsal part of the occipital arch adjacent to the foramen
magnum.
The exoccipital (Exo) forms part of the caudal wall of
the braincase (Fig. 7B). A process from the exoccipital
extends into the hyoid arch. The hyoid arch contains
ossification centers in the stylohyoid (Sth) and thyrohyoid (Thh, Fig. 7B,D), but the basihyoid cartilage (Bas
crt) is not ossified at this stage.
DISCUSSION
This study allows us to discuss in detail some adaptations that are of general interest in the development of
the skull in S. attenuata from stage 20 to stage 23 of
Thewissen and Heyning (2007). These adaptations relate
to key cranial anatomical elements of the cetacean skull.
Here, we will discuss telescoping of the skull, nasal
anatomy, and the development of the middle ear and ear
anatomy.
Telescoping
Telescoping in odontocetes is defined by the positioning of the maxilla and premaxilla in the skull (Miller,
1923; Kellogg, 1928a, 1928b). The premaxilla and the
ascending process of the maxilla override the frontal and
the parietal bones pushing dorsally and caudally (Miller,
1923; Oelschläger, 1990; Comtesse-Weidner, 2007). This
dorsal movement of anterior skeletal elements alters the
location of the sutures between specific bones (Miller,
1923). The premaxilla touches the supraoccipital bone
and the nasal, premaxilla, maxilla, parietal, and frontal
bones are all in close contact (Miller, 1923). The result of
telescoping in odontocetes is the reduction in the intertemporal region of the skull and it has been suggested
that this facilitates anatomical adaptations for echolocation (Kellogg, 1928a; Oelschläger, 1990). Telescoping
results in altering the shape of the anterior cranium and
flattening 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 development can be seen in four (LACM 94592, 94310, 94285,
94382) of the five Stenella fetuses presented in this
article.
In addition to telescoping, external bony nares position changes. This is directly and functionally related to
the 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 tip
of the rostrum to the top of the forehead (Klima, 1995;
Thewissen et al., 2009). The dorsal movement of the
external bony nares appears gradually in evolution in
protocetids and basilosaurids and throughout modern
whales (Thewissen et al., 2009). As the premaxilla and
maxilla extend dorsally, the external bony nares is
pushed dorsally to the top of the cranium leaving a thin
sliver of frontal bone exposed in adult odontocetes
(Miller, 1923).
The shifting of cranial bone position is unique to odontocete telescoping (Miller, 1923; Kellogg, 1928a). This
relative displacement of cranial bones is not present in
Eocene whales or mysticetes (Miller, 1923; Kellogg,
1928a) The mysticete maxilla cannot override the frontal
bone due to its two bony processes (Kellogg, 1928a). The
ascending process of the maxilla overlaps the frontal
bone while the infraorbital process of the maxilla lies
under the frontal bone securing the maxilla in position
(Kellogg, 1928a). Rostral movement of cranial bones
occurs in mysticetes with the posteriorly located occipital
bone pushing rostrally (Kellogg, 1928b). This rostral
shift in mysticetes is also called telescoping (Miller,
1923).
In S. attenuata, the maxilla does not override the frontal and parietal bones in the early stage 20 fetus (Figs.
2A,B and 3A,B), but the later fetuses do show evidence
of telescoping (Figs. 3C,D and 5–7). Specifically, the late
stage 20 (LACM 94592, Fig. 5) and the stage 21/22
(LACM 94310, Fig. 6) fetuses exhibit the beginning of
telescoping (Figs. 3C, 5D,and 6D). The premaxilla is
elongated rostrally in LACM 94592 (Figs. 3 and 5). The
maxilla reaches dorsally as far as the middle of the
orbit. The maxilla and the premaxilla are located dorsally and partly overlap the parietal and frontal bones
(Figs. 3C,D, 5A,B, and 6A,B). In stage 21/22, the gap
between the frontal bone and the maxilla is not visible
(Figs. 5D and 6D). Even less of the frontal bone is
exposed in the older fetuses (LACM 94285 and 94382,
stage 23) as telescoping is well underway.
Nasal Anatomy
The nasal anatomy of cetaceans is unique among
mammals (Klima, 1995). The median nasal cartilage, as
well as the bony elements of the rostrum, acts as a conduit for echolocation emissions (Cranford et al., 1996;
Klima, 1999). Klima (1999) suggested the median nasal
cartilage aids the growth of the embryonic rostrum in
length before the bony elements are in place. Histologically, the median nasal cartilage is different from the
cartilaginous nasal septa of land mammals due to the
high amount of fibrous cartilage and interwoven fiber
bundles (Klima, 1999).
The vomer is a thin triangular wedge of bone in the
palate of LACM 94592 (Fisg. 3D and 5A,C). The vomer
is rostrally almost as long as the maxilla and flares dorsoventrally 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 nasal
cartilage. The vomer grows in length as the maxilla and
premaxilla lengthen and the rostrum elongates.
The median nasal cartilage has the shape of an equilateral triangle and is one of the most conspicuous parts
of the dolphin skull in the early stage 20 fetus, LACM
94671 (Figs. 2A and 3B). The median nasal cartilage
flares dorsally and is elongated with the outgrowth of
the rostrum in late stage 20 and stages 21/22. This
lengthening can be seen in LACM 94310 (Fig. 6A). The
median nasal cartilage is continuous with the chondrocranium (Fig. 6A). The median nasal cartilage does not
completely reach to the rostral tip as the premaxillary
cartilage is still present at the very tip of the rostrum
even at stage 23 of development (Fig. 7A,B). There is
minor change in the median nasal cartilage after late
stage 20. The monkey lip dorsal bursae or phonic lips
(Au, 1993; Cranford et al., 1996; Berta et al., 2006) are
not visible in any of the fetal stages discussed here.
DEVELOPMENT OF THE SKULL OF S. attenuata
Ear Anatomy
The three middle ear ossicles (the malleus, incus, and
stapes) transmit sound from the tympanic membrane to
the inner ear (Williams et al., 1995). Lancaster (1990)
made theoretical predictions of the position of the middle
ear ossicles in transitional cetacean ears based on the
fossil record. Thewissen and Hussain (1993), Thewissen
et al. (2009), and Nummela et al. (2004, 2006) documented transitional morphologies in fossils such as pakicetids, remingtonocetids, protocetids, and basilosaurids.
Sound transmission characteristics differ between air
and water prompting evolutionary change in the anatomy and morphology of the middle ear of cetaceans
(Nummela et al., 2007). Fifty million years ago, pakicetids had middle ear anatomy that was more similar to
land mammals than modern cetaceans (Nummela et al.,
2004). Pakicetids have a small mandibular foramen and
lacked a mandibular fat pad, suggesting that these early
whales did not hear well in water (Thewissen and Hussain, 1993; Nummela et al., 2007). Ambulocetus, remingtonocetids, and protocetids have a large mandibular
foramen and, where known, middle ear ossicles that
morphologically are more similar to modern cetaceans
(Nummela et al., 2004, 2007). The 35 million year old
middle ear of basilosaurids is considered fully modern
(Nummela et al., 2004).
Echolocating cetaceans have a pachyosteosclerotic
tympanoperiotic complex that is isolated from the skull
by air-filled sinuses (Purves, 1966; Oelschläger, 1990;
Nummela et al., 2007; Cranford et al., 2010; Hemilä
et al., 2010). This isolation of the ear from the skull
allows for directional hearing in water and the sinuses
change volume during pressure changes when diving
(Oelschläger, 1990; Reidenberg and Laitman, 2008). The
isolation of the tympanoperiotic complex in archaeocetes
through modern cetaceans provides more movement of
the tympanic plate. This relays sound from the water,
through the mandible, to the middle ear ossicles for
hearing (Fleischer, 1978; Luo, 1998; Nummela et al.,
2007; Cranford et al., 2010; Hemilä et al., 2010). Isolation of the tympanoperiotic complex is not definitively
exhibited in the Stenella fetuses.
The involucrum is the thickened medial wall of the
tympanic bone in adults; the lateral wall is thin enough
to see light shine through (Nummela et al., 2007). This
morphology is present in the earliest whales, back to
pakicetids, and is characteristic of cetacean ears (Nummela et al., 2007; Thewissen et al., 2009). The small
tympanic ring is a U-shaped ridge of bone located on the
thin lateral wall of the tympanic bone. It is where the
tympanic ligament attaches (Oelschläger, 1990). None of
our five embryos have an involucrum and the tympanic
ring is not visible. The pharyngotympanic tube is not
visible in any of the fetal stages discussed here.
The middle ear ossicles of cetaceans form a chain
within the tympanic bone, as in land mammals, but the
orientation 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 in
cetaceans. The manubrium of the malleus is reduced in
length (Fraser and Purves, 1960; Purves, 1966; Oelschläger, 1990) and points ventrally extending in a parasagittal plane in land mammals. The cetacean incus is
orientated so the crus breve and crus longum are rotated
1755
and point medially (Fleischer, 1978; Oelschläger, 1990;
Kinkel et al., 2001). Kinkel et al. (2001) described the
embryology of S. attenuata ossicles based on histological
sections of specimens. The cetacean malleus and incus
were found to be rotated approximately 90 degrees
around the physiological axis of rotation (Thewissen,
1994; Kinkel et al., 2001). This is considerably more rotation than seen in Pakicetus, which is considered to be the
intermediate between land mammal ossicle orientation
and 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 turn
medially and elongate in LACM 94592 (Fig. 4C,D) exposing
the stapes. The malleus is also continuing to develop and
separate from Meckel’s cartilage in Fig. 4C and D.
The accessory ossicle is a middle ear structure distinct, but synostosed in mysticetes and odontocetes, as
well as some fetal artiodactyls (Luo, 1998; Mead and
Fordyce, 2009). The accessory ossicle is homologous with
the embryonic accessory ossicle in artiodactyls, which
develops into the processus tubarius and merges into
the bulla (Oelschläger, 1990; Luo, 1998). Embryonically
in odontocetes, the accessory ossicle changes in only
minor ways from its fetal shape (Fig. 4) to the adult
shape (Luo, 1998). The adult odontocete accessory ossicle
is actually more similar to a fetal mysticete accessory ossicle (Luo, 1998). In adult mysticetes, the accessory ossicle fuses with the anterior process of the petrosal
forming a gracile pedicle connecting but not synostosing
with the bulla or processus tubarius (Luo, 1998). The
accessory ossicle provides an anterior junction between
the tympanic bone and the periotic bone (Oelschläger,
1990) and is visible just rostral to the malleus in LACM
94592 (Fig. 4C,D). The function of this structure is not
part of the middle ear model as outlined by Nummela
et al. (2004, 2007) or Cranford et al. (2010).
CONCLUSION
Cleared and stained specimens provide a great
resource for studying morphological developmental
changes in vertebrates. Direct interpretation of anatomy
from bony and cartilaginous structures is imperative for
ontogenetic comparisons. Cleared and stained specimens
are more easily interpreted than serial histological sections and allow for morphological comparisons to fossils.
These morphological studies can help guide molecular
techniques, such as immunohistochemistry and in situ
hybridization, in understanding the protein and mRNA
expression in cartilage and bone.
ACKNOWLEDGEMENTS
We would like to thank Sharon Usip for all her help
in the lab and in the staining process.
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