Cranial Osteiology of the Hylid Frog, Smilisca baudini Part 1

Cranial Osteiology of the Hylid Frog, Smilisca baudini.

by Linda Trueb.

INTRODUCTION

The paucity of descriptive cranial anatomical work dealing with hylid frogs was pointed out by Trueb (1966) in her paper describing the cranial osteology of _Hyla septentrionalis_. Comparative studies on the cranial osteology of the genus _Smilisca_ (Duellman and Trueb, 1966), along with other more brief descriptions, reveal variation among cranial characters of hylids. Since these external characters have been useful in defining species, species groups, and genera, it seems worthwhile to pursue correlated studies on internal cranial structure. The following account dealing with the Neotropical tree frog, _Smilisca baudini_ Dumeril and Bibron, 1841, is the first published description of the internal cranial anatomy of a hylid frog, and supplements the recent account (Duellman and Trueb, 1966) of external cranial osteology of the same species. Comparative studies of hylid skulls are expected to yield information of taxonomic importance.

I am grateful to Richard J. Baldauf of Texas A & M University and William E. Duellman of the University of Kansas for critically reading the ma.n.u.script and offering helpful suggestions. The findings reported here result from research on Middle American hylids supported by a grant from the National Science Foundation (GB-1441) to William E.

Duellman.

Materials and Methods

The serial sections ill.u.s.trated beyond are from an adult male of _Smilisca baudini_ (KU 89924) having a snout-vent length of 53.0 mm.

and a head width (measured at angle of jaws) of 17.0 mm. The specimen was collected 5.2 kilometers east-southeast of Cordoba, Veracruz, Mexico. Transverse sections were cut at thicknesses of 10 and 15 microns on a rotary microtome and stained according to the technique described by Baldauf (1958). Cleared and stained specimens and dried skeletons also were used. Figure 1 is based on KU 68183-4 and Fig. 9 on KU 55614. All other drawings are made from KU 89924. In all cross-sectional figures, bone is represented by solid black, cartilage by stippling, and connective tissue by cross-hatching. Unless otherwise noted all descriptions are given in an anterior-posterior sequence.

Commonly accepted English terms are used. For example, dentary is used in preference to dentale and maxillary process instead of processus maxillaris. If no commonly accepted English term is available for a given structure, the Latin name is retained. For example, the cartilaginous plate separating the cavum princ.i.p.ale from the cavum medium is termed the lamina superior.

[Ill.u.s.tration: FIG. 1. Partially disarticulated skull (left frontoparietal and nasal removed) of _Smilisca baudini_, KU 68183, [Female] 4. Abbreviations: _al. proc._, alary process of premaxillary; _ant. sq._, anterior arm of squamosal; _epi. em._, epiotic eminence; _exocc._, exoccipital; _fpar._, frontoparietal; _fpar. fon._, frontoparietal fontanelle; _max._, maxillary; _nas._, nasal; _pal._, palatine; _pal. proc._, palatine process; _pasph._, parasphenoid; _pmax._, premaxillary; _pvom._, prevomer; _post, sq._, posterior arm of squamosal; _pro._, prootic; _pter._, pterygoid; _qj._, quadratojugal; _spmax._, septomaxillary; _sept, nas._, septum nasi; _spheth._, spnenethmoid; _vent, sq._, ventral arm of squamosal.]

DESCRIPTION OF INTERNAL CRANIAL OSTEOLOGY

Olfactory Region

_Alary cartilage._--The anterior end of the alary cartilage (_al. c._, Figs. 2-5) lies within the posterior concavity of the alary process (_al. proc._, Figs. 1-3) of the premaxillary (_pmax._). In posterior sections the cartilage a.s.sumes a dorsolateral position (Fig. 3), ventral and slightly lateral to the tectum nasi. The alary cartilage remains narrowly separated from the tectum nasi but fuses ventromedially with the septum nasi and forms a nearly complete cartilaginous capsule around the anterior end of the cavum princ.i.p.ale.

Posterior to the anterior end of the cavum medium and the lamina superior, the alary cartilage separates ventrally from the lamina. In subsequent posterior sections, the cartilage, arcuate in cross section, becomes progressively smaller and terminates at the level of the union of the medial and lateral recesses of the cavum inferior.

_Prenasal cartilages._--The superior prenasal cartilage is small; it lies adjacent to the posterodorsal surface of the alary process of the premaxillary, and anterior to the alary cartilage. The inferior prenasal cartilage (_inf. pnas. c._, Figs. 2-6, and 8) appears posterior to the appearance of the alary cartilage. The anterior terminus lies at the base of the alary process; the cartilage extends dorsally (Fig. 3) along the posterior surface of the alary process and then curves posterodorsally and joins the solum nasi medioventral to the posterior end of the septomaxillary (Fig. 8d).

_Tectum nasi._--The anterolateral corner of the tectum nasi (_tect.

nas._, Fig. 2) appears just posterior and dorsomedial to the anterior end of the alary cartilage. The anterior process is short; it fuses medially with the septum nasi forming a complete roof to the cavum princ.i.p.ale (Figs. 3 and 4). The oblique cartilage (_obl. c._) diverges laterally from the tectum nasi just posterior to the terminus of the alary cartilage (Fig. 6). Medially, the tectum nasi persists, overlaid by the nasal bone laterally.

_Septum nasi._--Posterior to the appearance of the septum nasi (_sept, nas._) and its union with the tectum nasi (Fig. 3), the septum abruptly expands across the width of the skull medial to the alary cartilage. The septum is entirely cartilaginous posterior to the level of the olfactory eminence, except for a small amount of secondary membranous ossification dorsomedially at a level anterior to the nasal bones. Perichondral ossification commences in the dorsal part of the septum nasi at the level of the olfactory eminence. Endochondral ossification first appears dorsally in the vertical part of the septum at the level of the internal nares. Ossification of dorsal parts of the septum precedes ossification of ventral parts. Perichondral ossification of the ventral part of the septum nasi is first noted at the level of transition between the planum antorbitale and solum nasi. Perichondral ossification gradually gives way to endochondral ossification posteriorly.

[Ill.u.s.tration: FIGS. 2-5. Transverse sections through anterior end of skull: 2) anterior level of inferior prenasal cartilage; 3) anterior level of internasal septum; 4) olfactory capsule at anterior level of cavum princ.i.p.ale; 5) olfactory capsule at anterior level of cavum inferior. Abbreviations: _al. c._, alary cartilage; _al. proc._, alary process of premaxillary; _cav. med._, cavum medium; _cav. prin._, cavum princ.i.p.ale; _cr. int._, crista intermedia; _inf. pnas. c._, inferior prenasal cartilage; _l.

inf._, lamina inferior; _l. sup._, lamina superior; _max._, maxillary; _pmax._, premaxillary; _r. etx. n. f._, ramus externus narium foramen; _r. med. n. f._, ramus medialis narium foramen; _rec. lat._, recessus lateralis; _sept. nas._, septum nasi; _sol.

nas._, solum nasi; _spmx._, septomaxilla; _tect. nas._, tectum nasi.]

[Ill.u.s.tration: FIGS. 6-7. Transverse sections through olfactory capsule: 6) posterior level of cavum medium; 7) anterior level of prevomer. Abbreviations: _cav. inf._, cavum inferius; _cav. med._, cavum medium; _cav. prin._, cavum princ.i.p.ale; _cr. sub._, crista subnasalis; _ext. nar._, external nares; _inf._, infundibulum; _inf. pnas. c._, inferior prenasal cartilage; _l. inf._, lamina inferior; _l. sup._, lamina superior; _max._, maxillary; _nas._, nasal; _ncl. dt._, nasolacrimal duct; _obl. c._, oblique cartilage; _p. fac._, pars facialis; _p. pal._, pars palatina; _pvom._, prevomer; _rec. med._, recessus medialis; _sept. nas._, septum nasi; _sol. nas._, solum nasi; _spmax._, septomaxillary; _tect. nas._, tectum nasi.]

_Nasal cavities and a.s.sociated structures._--The cavum princ.i.p.ale (_cav. prin._, Fig. 4) is the most anterior of the nasal cavities. It first appears within the capsule bordered dorsally by the tectum nasi, medially and ventrally by the septum nasi, and laterally by the alary cartilage. The cavity extends posteriorly within recesses of the sphenethmoid to the level at which the septum nasi terminates.

The cavum medium (_cav. med._, Fig. 5) lies ventral and slightly posterior to the anterior end of the cavum princ.i.p.ale. It appears slightly anterior to the septomaxillary at the level of the foramen ramus externus narium and ramus medialis narium. The appearance of the cavum medium within the ventrolateral extension of the septum nasi divides the latter into an upper component, the lamina superior (_l. sup._) lying between the cavum princ.i.p.ale and cavum medium, and a lower part, the lamina inferior (_l. inf._) lying ventral to the cavum medium. As the cavum medium increases in width in posterior sections, the lamina superior and lamina inferior lose their lateral connection.

The lateral part of the cavum medium diverges in the region of the external nares as the nasolacrimal duct (_ncl. dt._) and the cavum medium becomes confluent with the cavum princ.i.p.ale (Fig. 6). The posterior end of the cavum medium lies at the level of the posterior terminus of the septomaxillary.

Slightly posterior to the anterior end of the cavum medium the foramen for the ramus externus narium (_r. ext. n. f._) and ramus medialis narium (_r. med. n. f._) opens ventromedially into the floor of the septum nasi (Fig. 4). The ventral closure of the floor of the foramen completes the solum nasi, marks the anterior end of the recessus medialis of the cavum inferior, and differentiates the roof of the recess, the crista intermedia (_cr. int._), from the solum (Fig. 5).

The crista intermedia joins the laminae superior and inferior and joins them for a short distance to the septum nasi medially. The anterolateral part of the cavum inferior (_cav. inf._) lies ventrolateral to the cavum medium, and extends medially to join the medial recess. The fusion of the two recesses of the cavum inferior completely separates the lamina inferior from the solum nasi (Fig. 6).

Near the level of the union of the recessus lateralis and recessus medialis of the cavum inferior, the crista intermedia separates from the septum nasi, and the lamina superior diverges at its mid-width to accommodate the septomaxillary (_spmax._) (Figs. 5 and 6). The lateral remnant of the lamina superior and transition zone between the lamina superior and lamina inferior is short and is quickly replaced by connective tissue. Slightly posterior, the distal edge of the lamina inferior diverges laterally as a small process, which lies dorsal to the pars facialis (_p. fac._) of the maxillary. This part of the lamina inferior terminates posteriorly at the level of confluence between the cavum princ.i.p.ale and lateral recess of the cavum inferior.

Slightly posterior to the divergence of the crista intermedia from the septum nasi, the crista terminates, thereby separating the lamina superior and the lamina inferior from one another (Figs. 6 and 8). The lamina superior terminates at the level of the infundibulum (_inf._, Fig. 7), whereas the lamina inferior extends posterolaterally, increases greatly in depth and joins the laterally ascending oblique cartilage (_obl. c._) to form the planum terminale (_pla. ter._, Fig. 10).

The crista subnasalis (_cr. sub._, Fig. 6) differentiates from the lateral edge of solum nasi adjacent to the maxillary in sections just posterior to the confluence of the recessus medialis and the recessus lateralis. The crista persists as a rod of cartilage which gradually diminishes in size and terminates at the posterior level of the septomaxillary.

_The septomaxillary._--The septomaxillary (_spmax._, Fig. 9a-c) is a triradiate bone. The anterior terminus is a thin sliver of bone oriented horizontally between the cavum princ.i.p.ale and cavum medium and lateral to the lamina superior (Figs. 5 and 8a). This anterior ramus of the septomaxillary increases in size posteriorly and diverges medially into a medial ramus (_med. r. spmax._) and lateral ramus (_lat. r. spmax._, Fig. 9a-b) to accommodate the confluence of the cavum princ.i.p.ale and cavum medium (Figs. 6 and 8b-c). The small medial ramus is a.s.sociated with the distal end of the lamina superior whereas the lateral ramus lies dorsal to the lateral margin of the cavum medium. Just anterior to the anterior end of the nasolacrimal duct, the ventral ramus of the septomaxillary (_vent. r. spmax._, Fig. 9c) is present in cross-sections ventral to the cavum medium. The ventral ramus joins the horizontal and dorsal rami of the septomaxillary at the anterior end of the nasolacrimal duct. The medial branch terminates posteriorly at the level at which the cavum princ.i.p.ale joins the cavum inferior. The lateral ramus of the septomaxillary terminates posteriorly at the level at which the recessus medialis diverges from the recessus lateralis posteriorly and cavum princ.i.p.ale and recessus lateralis are confluent.

_Planum terminale._--Posterior to the infundibulum the lamina inferior and oblique cartilage join to form the planum terminale (_pla. term._) which lies lateral to the cavum princ.i.p.ale (Fig. 10). The lamina inferior diverges ventrally from the planum terminale anterior to the olfactory eminence. The planum terminale is restricted ventrally and terminates at the level of the olfactory eminence (_olf. em._, Fig. 11).

[Ill.u.s.tration: FIG. 8. Transverse sections through olfactory capsule in region of septomaxillary: _a_) anterior terminus of septomaxillary; _b_) medial divergence of septomaxillary; _c_) dorsal ramus of septomaxillary; _d_) posterolateral terminus of septomaxillary. Encircled numbers represent the nasal cavities as follows: 1) cavum princ.i.p.ale; 2) cavum medium; and 3) cavum inferius. Abbreviations: _al. c._, alary cartilage; _ant. spmax._, anterior end of septomaxillary; _cr. int._, crista intermedia; _dor. r. spmax._, dorsal ramus of septomaxillary; _ext. nar._, external nares; _inf. pnas. c._, inferior prenasal cartilage; _l.

inf._, lamina inferior; _l. sup._, lamina superior; _lat. r.

spmax._, lateral ramus of septomaxillary; _med. r. spmax._, medial ramus of septomaxillary; _nas._, nasal; _nlc. dt._, nasolacrimal duct; _obl. c._, oblique cartilage; _pvom._, prevomer; _sept.

nas._, septum nasi; _sol. nas._, solum nasi; _spmax._, septomaxillary; _tect. nas._, tectum nasi.]

[Ill.u.s.tration: FIG. 9. Septomaxillary drawn from cleared and stained specimen of _Smilisca baudini_, KU 55614: _a_) dorsal; _b_) ventral; _c_) lateral. In each example, the anterior end lies to the left. Abbreviations: _dor. r. spmax._, dorsal ramus of septomaxillary; _lat. r. spmax._, lateral ramus of septomaxillary; _med. r. spmax._, medial ramus of septomaxillary; _vent. r.

spmax._, ventral ramus of septomaxillary.]

_Anterior and posterior maxillary processes._--The anterior end of the anterior maxillary process (_ant. max. proc._) lies within the maxillary at the level of the posterior terminus of the planum terminale. The anterior maxillary process diverges medially from the maxillary (Fig. 13) and expands dorsally along the medial face of the pars facialis to meet the planum antorbitale just anterior to the transition zone between the latter and the solum nasi. Posterior to the transition zone, the planum antorbitale disappears and the posterior maxillary process is restricted ventrally along the pars facialis of the maxillary. Posteriorly the cartilage is a.s.sociated with the pterygoid, where it is known as the pterygoid process (_pter. proc._, Fig. 14).

_Planum antorbitale._--The anterior terminus of the planum antorbitale (_pla. ant._) lies medial to the ventrolateral part of the nasal and lateral to the internal nares (Fig. 12). It abruptly expands dorsally along the medial face of the nasal to join the tectum nasi dorsolaterally; somewhat posteriorly the planum antorbitale joins the anterior maxillary process ventrally at the posterior margin of the internal nares.

[Ill.u.s.tration: FIGS. 10-11. Transverse sections through posterior part of olfactory capsule: 10) region of planum terminale; 11) anterior region of olfactory eminence. Abbreviations: _cav. p._, cavum princ.i.p.ale; _max._, maxillary; _nas._, nasal; _nlc. dt._, nasolacrimal duct; _olf. em._, olfactory eminence; _p. fac._, pars facialis; _p. pal._, pars palatina; _pla. ter._, planum terminale; _pvom._, prevomer; _rec. lat._, recessus lateralis; _sept. nas._, septum nasi; _sol. nas._, solum nasi; _tect. nas._, tectum nasi.]

[Ill.u.s.tration: FIG. 12. Transverse section through the olfactory capsule in region of planum antorbitale. Abbreviations: _cav. prin._, cavum princ.i.p.ale; _int. nar._, internal nares; _max._, maxillary; _nas._, nasal; _olf. em._, olfactory eminence; _p. fac._, pars facialis; _p. pal._, pars palatina; _pal._, palatine; _pla. ant._, planum antorbitale; _pvom._, prevomer; _sept. nas._, septum nasi; _sol. nas._, solum nasi; _tect. nas._, tectum nasi.]

_External dermal bones a.s.sociated with the olfactory region._--The a.s.sociation of the premaxillary (_pmax._) to the nasal cartilages is described in preceding sections. The premaxillaries are separated from each other medially and from the maxillaries laterally by dense connective tissue. Anteriorly, the maxillary (_max._) bears a small palatine process (_pal. proc._, Fig. 1) and a long, delicate pars facialis (_p. fac._, Fig. 6), which terminates dorsally at the level of the lamina inferior. Posterior to the transition zone between the planum antorbitale and solum nasi the pars facialis is greatly reduced. The pars palatina (_p. pal._, Fig. 6) persists to the posterior part of the orbit.

The anterior end of the prevomer (_pvom._, Fig. 1) is a.s.sociated with the venter of the solum nasi at the level of the infundibulum just posterior to the incorporation of the inferior prenasal cartilage into the solum (Fig. 7). The prevomer expands dorsally around the distal end of the solum to provide a bony lateral support for the olfactory eminence (Figs. 10 and 11). A distal wing of the prevomer forms the bony anterior and medial margins of the internal nares.

The palatine (_pal._, Figs. 1 and 12) lies in connective tissue medial and adjacent to the pars facialis. At its maximum size the palatine forms the bony posterior margin of the internal nares and extends dorsomedially from the pars palatina to the distal part of the solum nasi.

The nasal (_nas._, Fig. 1) is a thin bone overlying the tectum nasi anteriorly (Fig. 7). It expands laterally to form a complete roof over the cavum princ.i.p.ale (Fig. 10). In the region of the internal nares, the nasal forms the lateral wall of the cavum princ.i.p.ale (Fig. 12).

Sphenethmoid Region

Posterior to the transition zone between the planum antorbitale and solum nasi, the sphenethmoid (_spheth._, Fig. 1) is fully ossified medially, the lateral parts of the bone at this level are only ossified perichondrally. The septum nasi persists at the anterior level of the orbit and terminates just anterior to the orbitonasal foramen (_orbnas. f._) and the anterior end of the parasphenoid (_pasph._, Fig. 13). The orbitonasal foramen is moderately large, has a complete bony margin, and is located at the dorsolateral corner of the braincase.

[Ill.u.s.tration: FIG. 13. Transverse section through sphenethmoid region at level of orbitonasal foramen. Abbreviations: _ant. max.

proc._, anterior maxillary process; _max._, maxillary; _orbnas. f._, orbitonasal foramen; _pasph._, parasphenoid; _spheth._, sphenethmoid.]

At the level of the orbitonasal foramen, the sphenethmoid is entirely ossified except for a small dorsolateral extension. This distal extension expands laterally in posterior sections as the braincase is increased to its maximum width at the mid-length of the orbit; the cartilaginous margin is retained throughout the length of the sphenethmoid.

The bony dorsomedial part of the sphenethmoid diverges, forming the anterior border of the frontoparietal fontanelle (_fpar. fon._, Figs.