Part 13

Pectoral Girdle.--The omosternum is large, ovoid, and cartilaginous; the sternum is a thin cartilaginous sheet deeply notched posteriorly and is not differentiated into episternal and xiphisternal elements. The coracoids are robust, twice as stout as the clavicles. The epicoracoidal cartilages overlap in the usual arciferal manner, except that they are fused anteriorly between the slender clavicles. The clavicles are strongly arched. The clavicle, coracoid, and scapula on each side form a bony articulation at the glenoid fossa. A bifurcation of the ventral end of the scapula results in a large glenoid foramen. The scapula is flat and expanded dorsally; the suprascapula is broad, flat, and calcified in large adults. In young specimens no distinct ossification of the cleithrum or ossification of endochondral centers are evident.

Arm and Hand.--The humerus is equally well-developed in both sexes and has a prominent lateral crest. The radius and ulna are completely fused. A bony prepollex is present in both sexes. The metacarpals are about equal in length. The phalangeal formula is 2-2-3-3; the terminal phalanges are claw-shaped.

Pelvic Girdle.--The ilia are long, slender, and slightly curved. A thin ridge projects laterally from the dorsal edge of the posterior one-half of each ilium. The ilial prominence is large and knoblike when viewed from above. The anterior edge of the ilial prominence is at the level of the anterior edge of the acetabular border. The dorsal acetabular expansion is small. The pubis is slender, and the ischium is elevated and robust.

Leg and Foot.--The slightly curved femur has a distinct crest proximally on the posterior surface. The nearly straight tibio-fibula is slightly longer than the femur. The tibial and fibial elements are completely fused but have a distinct cleft between them. A small foramen exists at the mid-length of the tibio-fibula. The fibulare (calcaneum) is much more robust than the tibiale (astragalus). The prehallux is large and flat. The metatarsals of the third, fourth, and fifth digits are equal in length; the metatarsal of the second is somewhat shorter, and that of the first is much shorter. The phalangeal formula is 2-2-3-4-3; the terminal phalanges are claw-shaped.

Developmental Cranial Morphology of Smilisca baudini

The following description of development of the skull of Smilisca baudini is based on the examination of 12 cleared and stained specimens. In table 3 the cranial bones are listed in the left hand column in the approximate order of their appearance in the young frogs. Across the top of the table selected specimens designated by developmental stage or snout-vent length are listed. It should be noted that although each individual, from left to right, has an increasing number of ossified bones, the correlation with increasing size is imperfect; the precise ages of the individuals are unknown.

The first bones to appear are the septomaxillaries, frontoparietals, part of the exoccipital, and the parasphenoid in developmental stage 40. The frontoparietals are represented by two slender ossifications dorsomedial to the orbits; the septomaxillaries are present as small ossifications anterior to the nasal capsules (Pl. 1A). The parasphenoid is present as a faint median ossification, and the exoccipital shows some ossification.

Table 3.--The Order of Occurrence of Cranial Ossifications in the Skull of Smilisca baudini. Where Numbers Are Divided by a Slash Mark, the Left and Right Symbols Correspond to the Left and Right Sides of the Skull, Respectively.

=====================+=====+=====+=====+=====+=====+=====+==== Bone |Stage|Stage|12.6 |13.9 |32.0 |27.0 |20.1 | 40 | 44 | mm. | mm. | mm. | mm. | mm. ---------------------+-----+-----+-----+-----+-----+-----+---- Frontoparietal | X | X | X | X | X | X | X Parasphenoid | X | X | X | X | X | X | X Septomaxillaries | X | X | X | X | X | X | X Exoccipitals | X | X | X | X | X | X | X Squamosals | -- | X | X | X | X | X | X Premaxillaries | -- | X | X | X | X | X | X Maxillaries | -- | X | X | X | X | X | X Nasals | -- | -- | X | X | X | X | X Pterygoids | -- | -- | X | X | X | X | X Vomers | -- | -- | -- | X | X | X | X Palatines | -- | -- | -- | X | X | X | X Quadratojugals | -- | -- | -- | X | X | X | X Ethmoid | -- | -- | -- | -- | X | X | X Columellas | -- | -- | -- | -- | X | X | X Supraorbital Flanges | -- | -- | -- | -- | -- | X | X Prooetics | -- | -- | -- | -- | -- | -- | X Vomerine Teeth | -- | -- | 1/1 | 4/3 | 5/5 | 3/3 | 5/4 Maxillary Teeth | -- | 0/7 | 3/5 | 6/5 |30/31|30/26|37/36 Premaxillary Teeth | -- | 2/4 | 3/3 | 5/5 | 7/6 | 8/6 | 8/7 ---------------------+-----+-----+-----+-----+-----+-----+----

The dentigerous bones are among the most rapidly developed, although not the first to appear. They are present in developmental stage 44 before metamorphosis is completed. The maxillaries bear a few teeth anteriorly and are ossified posteriorly to a point one-third of the distance from the anterior to the posterior edge of the orbit. Ossification lengthens the posterior termini of the maxillaries to the posterior edge of the orbit. In front of the anterior margin of the orbit, bone is proliferated dorsal to the main axes of the maxillaries and forms moderate dorsal maxillary flanges. The premaxillaries appear simultaneously with the maxillaries. Initially they are widely separated medially from each other, and laterally from the developing maxillaries; each bears two or three teeth, large dorsally blunt alary processes, and small palatine processes. The median and lateral edges of the prenasal processes lengthen heterochronously, causing the median edges to be longest and to lie slightly dorsal to the level of the septomaxillaries. After the maxillaries and premaxillaries develop, the vomers appear as small horizontal ossifications anterior to the parasphenoid. Ossification begins in the lateral flanges, then in the prevomerine processes, and lastly in the posterior dentigerous parts of the bones; the prevomerine processes are the last parts of the vomers to ossify completely.

Initially the frontoparietals are present as thin rods of ossification dorsomedial to the orbits; the frontoparietals extend from the anterior to the posterior end of the orbit by developmental stage 44. The anterior ends of the bones remain thin and pointed; ossification progresses medially from the midpoint of the length of the orbit and posteriorly to the level of the exoccipital; a median center of ossification joins the frontoparietals posteriorly, thereby forming the posterior border of the frontoparietal fontanelle. The supraorbital flanges of the frontoparietals do not appear until all other cranial bones are ossified, or nearly so. The most rapid ossification begins laterally at the posterior edge of the orbit and decreases anteriorly over the posterior half of the orbit. This differential rate of proliferation of bone results in the pattern of development of the supraorbital flanges shown in figure 7. The nasals appear as thin slivers of bone half way between the anterior ends of the frontoparietals and the end of the snout. As ossification proceeds the nasals assume a triangular shape in dorsal view. The anterior ends are pointed; the lateral margins are parallel to the maxillaries. The posteromedial points do not reach the lateral margins of the ethmoid, and the maxillary processes extend about three-fourths the distance from the bodies of the nasals to the maxillaries. Following the union of the frontoparietals posteriorly, the nasals widen anteriorly and are narrower at the midpoints of their long axes than anteriorly or posteriorly. With further ossification the maxillary processes extend to the maxillaries and form complete bony anterior margins to the orbits; the mid-parts of the nasals widen (Pl. 1B).

The parasphenoid is the first of the palatal bones to appear. At metamorphosis the bone is well developed; the anterior tip is situated just in front of the anterior edge of the orbit, and posteriorly the lateral processes extend laterally beyond the ossified parts of the auditory region. The pterygoids do not appear until metamorphosis, when ossification is evident in only the mid-parts of the posterolateral arms. Ossification follows in the mid-parts of the anterolateral arms and occurs last in the pterygoid pedicles. The palatines do not appear until all three arms of the pterygoids are at least partly ossified. Ossification proceeds rapidly from the maxillaries medially to the unossified ethmoid, which is the last of the cranial bones to appear. Initially it is extremely shallow; dorsally it is widely separated from the nasals, and ventrally the posterior margin meets the anterior point of the parasphenoid. In dorsal view, ossification proceeds anteriorly between the nasals and posteriorly, ventral to the frontoparietals; ventrally, ossification proceeds posteriorly dorsal to the parasphenoid.

The ventral arms of the squamosal and the supraoccipital region of the exoccipital are the first occipital bones to appear. Ossification follows in the regions of the semicircular canals and occipital condyles. The dorsal end of the ventral arm of the squamosal and the posterior arm of the squamosal ossify as a unit at the same time the quadratojugal appears. Shortly thereafter the anterior arm of the squamosal ossifies, the distal part of the columella appears, and the anterior and lateral parts of the auditory region ossify.

The angular and dentary of the lower jaw appear concurrently with the dentigerous bones. Initially, the angular is short and broad; the articular surface is absent, and the anterior end is slightly overlapped by the dentary. The mentomecklians do not ossify until approximately the same time that the quadratojugal appears in the upper jaw.

Comparative Osteology

The genus Smilisca is characterized by the following combination of cranial osteological characters: (1) A large amount of bone is involved in the skull and a minimal amount of cartilage and/or secondarily ossified cartilage; co-ossification is absent. (2) The skulls are uniformly broad with angular lateral margins, and truncate anteriorly. (3) An internasal septum and quadratojugals are present. (4) A well-developed squamosal minimally extends one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally is separated from the maxillary by a suture. (5) The ethmoid is large; the distance between the anterior end of the ethmoid and the anterior edge of the premaxillary varies between 15 and 20 per cent of the total length of the skull.

On the basis of cranial osteology two species-groups can be recognized within the genus Smilisca. The sordida group, comprising S. sordida and puma, is characterized by a broad skull in which the lateral margins of the maxillaries are relatively straight anterior to the orbit. The moderate-sized nasals are rounded anteriorly, and bear relatively short, sometimes blunt, maxillary processes. The long axes of the nasals are not parallel to the maxillaries. The ethmoid is proportionately small in the sordida group. The bony part of the ethmoid terminates near the anterior edge of the orbits and does not extend anteriorly between the nasals; the entire anterior margin of the ethmoid is separated from the nasals by cartilage. The squamosals are generally small. They are narrow in dorsal view, and minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally, two-thirds the distance. The tegmen tympani are relatively small (Fig. 8).

In contrast to the tendency for reduction of cranial parts in the sordida group, the baudini group, constituted by S. cyanosticta, phaeota, and baudini, is characterized by more ossification of the cranial elements. The skull is broad; the lateral margins are less angular and are gently curved, rather than straight as in the sordida group. The nasals tend to be larger with the long axes parallel to the maxillary. Anteriorly the nasals are pointed, and posteriorly they bear long, delicate palatine processes extending to the maxillary. The ethmoid is fully ossified, extends anteriorly between the nasals, and laterally is separated by a suture from the nasals if the latter are fully ossified. The squamosals are large, and wide in dorsal view. They minimally extend one-fourth the distance from the dorsal end of the quadrate to the maxillary, and maximally are sutured to the maxillary. The tegmen tympani are massive.

Smilisca sila is intermediate between the two species-groups described. The skull is broad; the lateral margins are gently curved, and have a pronounced angularity just anterior to the palatines which results in a broad, truncate snout. The nasals are moderate in size; because of the anterior angularity of the lateral margins, the long axes of the nasals lie parallel to the maxillary. The nasals are only slightly pointed anteriorly, and posteriorly they bear short, blunt palatine processes and medial processes in contact with the lateral corners of the ethmoid. The ethmoid is fully ossified, but does not extend anteriorly between the nasals. The squamosals are moderate in size and extend one-fourth the distance from the dorsal end of the quadrate to the maxillary. The tegmen tympani are relatively large, but proportionately short.

The cranial characters utilized in the analysis of species groups (general shape, nature of the nasals, ethmoid, squamosals, and tegmen tympani), together with other characters, such as the relative height and shape of the prenasal processes, the extent of the internasal septum, and the nature of the vomers, frontoparietals, maxillaries and pterygoids are useful in distinguishing the various species (Table 4, Fig. 8), as well as in establishing relationships within the species-groups.

Within the sordida group, S. sordida and S. puma can be distinguished by the following characters: The bony part of the ethmoid terminates posterior to the anterior edge of the orbit and is thus widely separated from the nasals by cartilage in S. puma. In S. sordida the bony part of the ethmoid always terminates at a level equal to, or slightly in front of the anterior edge of the orbit; therefore, less cartilage exists between the ethmoid and nasals in S. sordida than in S. puma. The width of the premaxillary comprises about 30 per cent of the width of the skull in S. sordida and 20 per cent in S. puma. The proportion of the length of the skull anterior to the bony part of the ethmoid in S. sordida is approximately 21 per cent, as compared with about 29 per cent in S. puma. The prenasal processes are convex in S. sordida and straight in S. puma.

The marked ontogenetic variation in S. sordida is considered in more detail in the account of that species, but it is pertinent to the present discussion to note that with respect to some features of the skull some young breeding specimens of S. sordida are intermediate in appearance between large females of S. sordida and adults of S. puma. In some breeding males (usually the smaller individuals) of S. sordida the bony part of the ethmoid terminates at the anterior edge of the orbit and is widely separated from the nasals by cartilage. In small individuals S. sordida, especially in males, and in adults of S. puma the tegmen tympani are relatively short, whereas in adult females of S. sordida these elements are long and slender. In the smaller specimens of S. sordida and in S. puma the squamosal is small; it extends only about one-fourth of the distance to the maxillary in the smaller S. sordida and about one-half the distance in S. puma. The more massive squamosal in large adult females of S. sordida extends at least two-thirds of the distance to the maxillary.

Table 4.--Comparative Cranial Osteology of Smilisca.

===============+==============================+======================= Character | S. baudini | S. cyanosticta ---------------+------------------------------+----------------------- | | Alary Processes| Four times as high as | Three times as high | lateral wing of premaxillary;| as lateral wing of | anteriorly | premaxillary; | convex. | anteriorly | | convex. | | Nasals | Long, wide anteriorly, | Long, widest | narrowing posteriorly; | posteriorly; | attached to ethmoid. | attached to | | ethmoid. | | | | | | Ethmoid | Long; entirely ossified; | Long, entirely | smooth margins. | ossified; | | smooth margins. | | Frontoparietal | Small, ovid fontanelle | Large fontanelle, two | present or absent; | and one-half times as | long, pointed postorbital | long as wide; narrow | processes curving | supraorbital flanges | along posterior | with irregular margins. | border of orbit. | | | Squamosal | Large: anterior arm | Large; anterior arm | in contact with maxillary. | in contact with | | maxillary. ---------------+------------------------------+------------------------

TABLE 4 (Continued) ===============+=============================+========================= Character | S. phaeota | S. puma ---------------+-----------------------------+------------------------- | | Alary Processes| Two and one-half | Two times as high as | times as high as lateral | lateral wing of | wing of premaxillary; | premaxillary; | anteriorly convex. | straight. | | | | Nasals | Long, widest anteriorly | Short, narrow, not | and posteriorly, | attached to ethmoid. | bearing posteromedial | | process; not attached | | to ethmoid. | | | | | Ethmoid | Long, entirely ossified; | Short, about two-thirds | smooth margins. | ossified; irregular | | margins. | | Frontoparietal | Fontanelle absent; | Keyhole-shaped fontanelle; | large supraorbital | smooth margins; | flanges having | flanges absent. | straight edges and extending| | posterolaterally. | | | | | Squamosal | Large; anterior arm | Small; anterior arm | extending 1/2-2/3 way | extending 1/2 way to | to maxillary. | maxillary. ---------------+-----------------------------+--------------------------

TABLE 4 (Continued) ===============+===========================+============================ Character | S. sila | S. sordida ---------------+---------------------------+---------------------------- | | Alary Processes| One and one-half | Two and one-half | times as high as lateral | times as high as lateral | wing of premaxillary; | wing of premaxillary; | straight. | slightly convex | | anteriorly. | | Nasals | Short, wide, bearing | Moderately long narrowest | small posteromedial | anteriorly and | processes; not attached | posteriorly; not attached | to ethmoid. | to ethmoid. | | | | | | Ethmoid | Moderately long; entirely | Short; one-half to entirely | ossified; smooth | ossified; irregular | margins. | margins. | | Frontoparietal | Large, ovoid fontanelle; | Large, elongate fontanelle; | smooth margins; | smooth margins; | flanges absent. | flanges absent. | | | | | | | | Squamosal | Moderately large; anterior| Moderately small; anterior | arm extending | arm extending | 1/4 way to maxillary. | 1/4-2/3 way to maxillary. ---------------+---------------------------+----------------------------

Within the baudini group, the skull of S. cyanosticta is the most generalized of the three species; the cranial characters are intermediate between S. phaeota and S. baudini. The lateral margins of the skull in S. cyanosticta are gently curved, and have an angularity anterior to the palatine-maxillary suture; the anterior margins are less angular in S. phaeota, which has a broader snout. Posteriorly in S. baudini the margins are slightly curved medially, and the greatest width of the skull is between the quadratojugal-maxillary sutures on either side of the skull. The frontoparietals of S. cyanosticta bear slightly irregular lateral margins and a large fontanelle. There is a tendency for obliteration of the fontanelle with increasing age in both S. baudini and S. cyanosticta; the lateral margins of the frontoparietals bear large supraorbital flanges in both of these species. In S. phaeota the flanges are most prominent; they extend posterolaterally with straight margins along two-thirds of the length of the orbit and terminate in rather blunt points. The broad interorbital flanges result in a relatively broad external interorbital distance. In S. baudini the flanges are curved posterolaterally around the orbit and terminate in sharp, thin points. The tegmen tympani of all three species are massive. In S. cyanosticta the prooetics slope posteriorly, whereas they slope anteriorly in S. baudini and S. phaeota.

The skulls of S. cyanosticta and S. baudini are alike in certain respects. The squamosals of both species are large and connected to the maxillary by a bony connection; the squamosals of S. phaeota are large, but extend only two-thirds of the distance from the dorsal end of the quadrate to the maxillary. In S. baudini and S. cyanosticta the nasals are separated throughout their lengths from the ethmoid, whereas the nasals of S. phaeota are separated from the ethmoid by cartilage. The latter separation is due to an incomplete ossification of the nasals in S. phaeota. The bony part of each nasal is constricted in the middle of the long axis of the bone, and the nasals are widest anteriorly; posteriorly each nasal bears a medial process, which is narrowly separated from the lateral edge of the ethmoid.