Download Comparative cranial osteology of fossorial lizards from the tribe

JOURNAL OF MORPHOLOGY 271:1352–1365 (2010)
Comparative Cranial Osteology of Fossorial Lizards
From the Tribe Gymnophthalmini (Squamata,
Gymnophthalmidae)
Juliana G. Roscito* and Miguel T. Rodrigues
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo-SP, Brazil
ABSTRACT Squamates (lizards, snakes and amphisbaenians) are represented by a large number of species
distributed among a wide variety of habitats. Changes in
body plan related to a fossorial habit are a frequent trend
within the group and many morphological adaptations to
this particular lifestyle evolved convergently in nonrelated species, reflecting adaptations to a similar habitat.
The fossorial lifestyle requires an optimal morphological
organization for an effective use of the available resources. Skeleton arrangement in fossorial squamates reflects
adaptations to the burrowing activity, and different
degrees of fossoriality can be inferred through an analysis
of skull morphology. Here, we provide a detailed description of the skull morphology of three fossorial gymnophthalmid species: Calyptommatus nicterus, Scriptosaura
catimbau, and Nothobachia ablephara. J. Morphol. 271:
1352–1365, 2010. Ó 2010 Wiley-Liss, Inc.
KEY WORDS: body plan; fossoriality; gymnophthalmidae;
skull morphology
INTRODUCTION
Squamates comprise approximately 8,400 species and represent a diverse group of animals,
which exhibit several adaptative phenotypes
related to the biogeographic context in which each
group evolved. These adaptations range from differences in habitat use and diet to differences in
size and body plans (Vitt et al., 2003).
Convergent evolution of morphological traits is
an often observed phenomena within the group
(Wiens and Slingluff, 2001), the most obvious being
the repeated evolution of a snake-like body plan
related to fossorial habits, involving body lengthening and limb reduction (Brandley et al., 2008; Gans,
1975; Greer, 1991; Wiens et al., 2006). According to
Wiens et al. (2006), a snake-like body plan has
evolved independently about 25 times, and even in
the same family, (e.g., anguids, gymnophthalmids,
and scincids) intermediate or extreme cases of body
elongation and limb reduction are found among
closely related species or within the same genus
(Pellegrino et al., 2001; Shapiro, 2002; Skinner
et al., 2008; Wiens and Slingluff, 2001).
The transition to fossoriality reflects an adaptative complex, which involves morphological modifiÓ 2010 WILEY-LISS, INC.
cations in skeletal patterns related to elongation of
the body, reduction/loss of limb bones, and skull
modifications, such as loss of elements and excessive growth and robustness of others, associated
with skull consolidation (Greer, 1991; Lee, 1998;
Rieppel, 1996; Tarazona et al., 2008).
Gymnophthalmidae (Estes et al., 1988) comprises an assemblage of 42 genera of small lizards
distributed throughout Central and South America
(Rodrigues et al., 2007), many of which are fossorial burrowers with elongated trunks and reduced
or lost limbs. These modifications toward the evolution of snake-like body plans have originated independently several times during the evolutionary
diversification of the family (Pellegrino et al.,
2001).
Within the Gymnophthalmidae, a monophyletic
group of nine genera which is taxonomically
known as the tribe Gymnophthalmini (Pellegrino
et al., 2001; Rodrigues, 1991, 1995; Rodrigues and
dos Santos, 2008), shows a clear and noticeable evolutionary trend related to a transition from a lacertiform to a serpentiform body plan. The basal
genera (Tretioscincus, Micrablepharus, Gymnophthalmus, Procellosaurinus, Vanzosaura, and Psilophthalmus) are diurnal, lizard-like in shape, and
have well-developed limbs and digits and tails longer than body length, while the derived genera
(Nothobachia, Scriptosaura, and Calyptommatus)
are fossorial, show adaptations to life in sand, and
are characterized by a snake-like shape, with
extremely elongated body, tails shorter than body,
Contract grant sponsors: Fundação de Amparo à Pesquisa do
Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq).
*Correspondence to: Juliana G. Roscito, Departamento de Zoologia, Instituto de Biociências-Universidade de São Paulo, Cidade
Universitária, Rua do Matão, Trav. 14, no. 321, São Paulo-SP, Brazil
CEP 05508-090. E-mail: [email protected]
Received 10 March 2010; Revised 21 April 2010;
Accepted 5 May 2010
Published online 26 August 2010 in
Wiley Online Library (wileyonlinelibrary.com)
DOI: 10.1002/jmor.10878
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
and limbs reduced or absent; Calyptommatus is
the only nocturnal genus of this radiation.
The digit pattern in the Gymnophthalmini is represented by a progressive reduction/loss of phalanges
and digits along its evolutionary history. The six lizard-like genera all have four well-developed limbs.
The forelimbs of Tretioscincus, Micrablepharus,
Gymnophthalmus, Procellosaurinus, Vanzosaura,
and Psilophthalmus, all have three, four, five, and
three phalanges in Digits II, III, IV, and V respectively, and in Digit I is observed a progressive
reduction in the number of phalanges, with two
small phalanges in Tretioscincus, one vestigial phalange in Micrablepharus and Gymnophthalmus, and
no phalanges in the three latter genera. The hind
limbs have five digits with a phalangeal formula of
2:3:4:5:4 (Rodrigues, 1995). In contrast, the three
snake-like genera show more severe degrees of limb
reduction: Nothobachia has a styliform forelimb and
a hind limb with two small digits and Scriptosaura
and Calyptommatus have no visible forelimb and a
styliform hind limb. These three genera have bodies
much more elongated than those of the other six
lacertiform genera, showing a snout-vent length
(SVL) larger than tail length (due to a increase in the
number of presacral vertebrae; Rodrigues, 1995).
Also, in the fossorial and snake-like genera, the
eyes are reduced, there is no external ear opening,
the snout is sharp, and the skull is more compact
than that of the diurnal and nonfossorial genera,
these characters reflecting the burrowing lifestyle.
Furthermore, Calyptommatus shows unique features of some skull bones not present in any of the
other fossorial genera (Rodrigues, 1995).
In this article, we provide a detailed comparative description of the adult skeletal morphology of
the skull and axial skeleton in Calyptommatus nicterus, Scriptosaura catimbau, and Nothobachia
ablephara and discuss the morphological adaptations that reflect the different degrees of fossoriality observed in these species.
MATERIAL AND METHODS
The description is based on eight adult specimens of Calyptommatus nicterus (Rodrigues, 1991) obtained at Vacaria, State of
Bahia, Brazil (Museu de Zoologia da Universidade de São Paulo
[MZUSP] 79549, MZUSP 79550, MZUSP 79551, MZUSP 79552,
MZUSP 79553, MZUSP 79554, Miguel Trefaut Rodrigues [MTR]
886837, and MTR 16767), two adults of Scriptosaura catimbau
(Rodrigues and dos Santos, 2008) obtained at Parque Nacional do
Catimbau, Buique, State of Pernambuco, Brazil (MTR 16777 and
MTR 16778), and five adults of Nothobachia ablephara
(Rodrigues, 1984) obtained at Alagoado, State of Bahia, Brazil
(MZUSP 79573, MZUSP 79574, MTR 16774, MTR 16775, and
MTR 10378). The specimens are deposited in the collection of
MTR and the MZUSP.
All specimens were cleared and double stained for bone and cartilage following an adaptation of protocols from Potthoff (1984),
Taylor and Van Dyke (1985), Song and Parenti (1995), and
Springer and Johnson (2000). The material was examined using
an Olympus stereomicroscope. Digital pictures, with corresponding scales, were taken with a digital camera attached to the stereo-
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microscope. Schematic drawings were made using the digital
images as shapes. For all specimens, SVL was measured, and
head length was measured from the anterior tip of the snout to the
back of the occipital condyle. The anatomical terminology follows
Bell et al. (2003), Torres-Carvajal (2003), Tarazona et al. (2008),
Evans (2008), and Guerra and Montero (2009). Abbreviations are
as follows: 1ctb, first ceratobranchial; 2ctb, second ceratobranchial;
1epb, first epibranchial; 2epb, second epibranchial; aaf, anterior
auditory foramen; al.p, alar process; alp.f, anterolateral process of
the frontal; alp.m, anterolateral process of the maxilla; amp.crn,
anteromedial process of the coronoid; amp.m, anteromedial process of the maxilla; ang, angular; ap.pm, alveolar plate of the premaxilla; asc, anterior semicircular canal; bh, basihyal; bo, basioccipital; bpt.p, basipterygoid process; ch.g, choanal groove; cm, columella; crn, coronoid; d, dentary; dp.p, descending process of the
parietal; ecp, ectopterygoid; eph, epihyal; ept, epipterygoid; exc.a,
exoccipital area; f, frontal; fcf, facial foramen; fo, fenestra ovalis;
fp.m, facial process of the maxilla; ftb, frontoparietal tab ; gh, glossohyal; hc, hyoid cornu; hsc, horizontal semicircular canal; j, jugal;
lgc, lagenar cavity; m, maxilla; m.ps, maxillary palatal shelf;
mp.pm, maxillary process of the premaxilla; n, nasal; np.pm, nasal
process of the premaxilla; obf, orbitosphenoid; oc, occipital condyle;
op.a, opisthotic area; or, occipital recess; p, parietal; paa complex,
prearticular-articular complex; paf, posterior auditory foramen;
pbs, parabasisphenoid; pf, postfrontal; pl, palatine; plp.f, posterolateral process of the frontal; pm, premaxilla; pm.ps, premaxillary
palatal shelf; pmp.crn, posteromedial process of the coronoid; po,
postorbital; pof, postorbitofrontal; pp, postparietal process; ptf,
posttemporal fenestra; prf, prefrontal; prp, paroccipital process;
psc, posterior semicircular canal; pss, planum supraseptale; pt,
pterygoid; q, quadrate; qp.pt, quadrate process of the pterygoid; so,
supraoccipital; spl, splenial; spm, septomaxilla; sq, squamosal; sra,
surangular; st, supratemporal; tgn, trigeminal notch; tr, trabecula;
v, vomer; vf, vagus foramen; vtc, vestibular cavity; XII, foramina
for the hypoglossal nerve roots.
RESULTS
General Features of the Skull
The skulls of Calyptommatus nicterus (Fig. 1),
Scriptosaura catimbau (Fig. 2) and Nothobachia
ablephara (Fig. 3) measure 6 mm in length, corresponding approximately to 10.5, 11, and 11.5% of
the SVL (average SVL of 5.7, 5.5, and 5.2 cm,
respectively). All are relatively elongated, but the
skull of C. nicterus is much wider than that of the
other two species; the snout is sharp in all three.
The orbital area of C. nicterus is smaller than that
observed in the other two species, and its palate
and the lateral wall of the skull posterior to the
orbits are completely closed by extensions of the
bones that form these regions; in S. catimbau,
however, a small ventral projection from the parietal bone is observed anterior to the epipterygoid,
in contrast with the almost imperceptible projection in N. ablephara. In S. catimbau and N. ablephara, no complex articulations are observed
between elements, whereas the bones of the skull
of C. nicterus are tightly articulated with each
other, making the skull very compact.
Premaxilla. The premaxilla forms the anterior
tip of the snout. It comprises an alveolar portion
and a nasal process. The alveolar plate is thicker
in C. nicterus and thinner in N. ablephara, with
that of S. catimbau falling in between; it carries
Journal of Morphology
1354
J.G. ROSCITO AND M.T. RODRIGUES
the dorsal margin of the nares and to overlap the
nasals and the anterior margin of the frontal posteriorly. In C. nicterus, the nasal process of the
premaxilla overlaps only a minor portion of the
anteromedial margin of the nasals (Fig. 1A),
whereas in S. catimbau and N. ablephara, it covers a greater portion of them (Figs. 2A and 3A).
Maxilla. The maxilla is a large element forming
most of the lateral surface of the skull anterior to
the orbit. The anterior end is represented by a bifurcated premaxillary process, divided into a slender anterolateral part that articulates with the
maxillary process of the premaxilla and a larger
anteromedial part that contacts the dorsal surface
of the palatal shelf of the premaxilla and forms
the ventral floor of the nares.
Ventrally, the anteromedial process is continued
by a well-developed maxillary palatal shelf, which
is aligned with the lateral margin of the vomer
Fig. 1. C. nicterus, drawing of the skull in dorsal (A), lateral (B).
and ventral (C) views. Sutures are represented by dashed lines;
shaded area in C represents roof of the skull. Scale bar 5 1 mm.
8–9, 9, and 7 unicuspid teeth, respectively, positioned along its ventral margin (Figs. 1C and 4A;
3C and 6B; 2C and 5B, respectively). Dorsally and
posterior to the teeth row, the V-shaped palatal shelf
contacts the vomer medially and the anteromedial
portion of the premaxillary process of the maxilla.
Laterally, the maxillary process of the premaxilla
articulates with the anterolateral portion of the premaxillary process of the maxilla. In C. nicterus and
S. catimbau, this maxillary process is bifurcated
into dorsal and ventral rami, supporting the anterior end of the maxilla between them (Fig. 5C); in
N. ablephara, the maxillary process is simple and
contacts only the internal and ventral surface of the
anterior end of the maxilla (Fig. 6G).
The broad nasal process of the premaxilla
projects from the medial part of the alveolar plate
to overlap part of the anterior margin of the frontal. It is slender anteriorly, then widens to form
Journal of Morphology
Fig. 2. S. catimbau, drawing of the skull in dorsal (A),
lateral (B), and ventral (C) views. Shaded area in C represents
roof of the skull. Scale bar 5 1 mm.
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
Fig. 3. N. ablephara, drawing of the skull in dorsal (A), lateral (B), and ventral (C) views. Scale bar 5 1 mm.
and ends at the region of the choana, being overlapped dorsally by the palatine and contacting the
external margin of the ectopterygoid (Figs. 1C, 2C,
and 3C); the palatine process of the prefrontal
stands on the dorsal surface of the shelf. The maxillary alveolar region bears six unicuspid teeth in
C. nicterus (Figs. 1C and 4A), eight in N. ablephara (Figs. 2C and 6B) and 9–10 in S. catimbau
(Figs. 2C and 5B).
The facial process of the maxilla forms the posterior margin of the naris and contacts anterodorsally and the anterolateral process of the frontal in
N. ablephara (Fig. 3B) and S. catimbau (Fig. 5A);
in C. nicterus, the anterolateral process of the
frontal is completely overlapped by the nasal, and
thus the facial process of the maxilla contacts
directly the dorsal extremity of the nasal (Fig. 1B).
Posterodorsaly, the facial process contacts the prefrontal, overlapping its anterior process, and posteroventrally, the maxillary orbital process underlies the anterior process of the jugal.
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Nasal. The nasal is approximately trapezoidal
in shape and is smaller in C. nicterus compared
with the other two species. It meets the nasal process of the premaxilla medially, which completely
separates it from its counterpart at the midline,
and posteriorly (Fig. 1A). In N. ablephara and S.
catimbau (Figs. 2A and 3A), in which an anterolateral process of the frontal is exposed, the nasal
meets this process posteriorly and laterally. The
anterior and lateral margins of the nasal contact
the facial process of the maxilla and form the dorsal margin of the nares.
Prefrontal. The prefrontal forms the anterior
and part of the dorsal margins of the orbit, protecting it anteriorly through strong connections
with neighboring elements. This element is composed of an anterior process, represented by a
broad sheet of bone that is overlapped by the facial
process of the maxilla, a posterodorsal process contacting the anterior and lateral margins of the
frontal and extending up to the middle of the orbit,
and a ventral palatine process contacting the anterior border of the palatine medially and the dorsal
surface of the maxillary palatal shelf laterally. A
huge lacrimal foramen is observed between the
internal wall of the facial process of the maxilla
and the ventral process that rests on the maxillary
palatal shelf. The ventral end of the prefrontal
meets the anterior process of the jugal.
The lacrimal flange is represented by a posteriorly directed projection, quite broad in N. ablephara (Fig. 3B) and smaller in S. catimbau
(Fig. 2B), when compared with that of the former;
in C. nicterus, no lacrimal flange is observed
(Figs. 1B and 4G).
In C. nicterus, the posterodorsal process of the
prefrontal is placed beneath the lateral margin of
the frontal and is, thus, not visible in dorsal view.
Both this process and the frontal participate in
the formation of the dorsal margin of the orbit.
The process is clearly seen, though, lateral to the
margin of the frontal in the other two species,
forming alone the anterior part of the dorsal margin of the orbit (Fig. 6A).
Jugal. The jugal is slightly sigmoidal in shape.
It forms the ventral and part of the posterior margins of the orbit. Its anterior maxillary process
contacts the ventral end of the prefrontal and is
supported ventrally by the orbital process of the
maxilla; its dorsal temporal process contacts the
ventral margin of the postorbital. Medially, the jugal contacts the lateral margin of the ectopterygoid.
In N. ablephara, the jugal is a slender element
with relatively sharp extremities and a more
robust middle portion (Fig. 6E). In C. nicterus, the
jugal is stouter and triradiate in shape, with a
robust posterior free process (Figs. 4D,G). In S.
catimbau, the jugal resembles that of N. ablephara
but has a small protuberance at the same place
Journal of Morphology
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J.G. ROSCITO AND M.T. RODRIGUES
Fig. 4. C. nicterus, cleared and stained skulls. (A) Ventral view of the anterior portion of the skull. (B) Posterolateral view of
the braincase; anterior to the left. (C) Braincase in lateral view; quadrate not represented. (D) Detail of the jugal in lateral view; anterior to the right. (E) Medial surface of the postorbitofrontal in lateral view; anterior to the left. (F) Descending process of the parietal
and alar process of the prootic in lateral view; anterior to the right. (G) Detail of the lateral surface of the skull anterior to the orbit;
anterior to the right. (H) Frontal in ventral view showing its well-developed cristae cranii (indicated by asterisk); anterior to the left.
Scale bars 5 0.5 mm.
where the posterior process of C. nicterus is
observed (Fig. 2B).
Frontal. The frontal forms the anterior skull
roof between the orbits. In C. nicterus, which has
a reduced orbit, the frontal is wider than those of
N. ablephara and S. catimbau, where the frontal
is narrower and longer. Its anterolateral margin
bears an anterolateral process with a distinct
facet for the nasal, by which it is completely overlapped dorsally in the articulated skull of C. nicterus (Fig. 1A). In N. ablephara and S. catimbau,
the nasal does not cover the entire anterolateral
process of the frontal (Figs. 2A and 3A), leaving
it exposed to separate the nasal from the dorsal
tip of the facial process of the maxilla.
The lateral margin of the frontal contacts the
posterodorsal process of the prefrontal anteriorly
Journal of Morphology
and the anterior end of the postfrontal (or postorbitofrontal, as is the case in C. nicterus) posteriorly. The cristae cranii originate at each lateral
margin and contact the posterodorsal process of
the prefrontal. They are short and slightly
curved medially, except in C. nicterus, where the
cristae are well developed and highly curved (but
do not contact each other at the midline; Fig.
4H), being supported by the ventral palatine process of the prefrontal and by the dorsal surface
of the palatine. The cristae cranii encapsulate
and protect the olfactory bulb.
At the posterior end of the lateral margin of the
frontal, a small posterolateral process contacts the
postfrontal. In N. ablephara, this process is sharp
(Fig. 3A), in S. catimbau, it is slightly rounded
(Fig. 2A), and in C. nicterus, there is no such pro-
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
1357
Fig. 5. S. catimbau, cleared and stained skulls. (A) Anterior part of the skull in dorsal view; anterior to the left. (B) Ventral view of
the anterior part of the palate; anterior to the left. (C) Articulation between premaxilla and maxilla in lateral view; anterior to the right.
(D) Lateral view of the middle portion of the skull, with detail of the descending process of the parietal; anterior to the right. (E) Braincase in lateral view; quadrate not represented. (F) Orbitosphenoid in dorsal view; anterior to the top. Scale bars 5 0.5 mm; except in C in
which scale bar 5 0.25 mm.
cess (Fig. 1A). This process is distinct from the
posteromedial process (frontoparietal tab) next to
it. These tabs are longer in N. ablephara and S.
catimbau than in C. nicterus and represent broad
areas of contact with the corresponding tabs of the
parietal, forming an ample area of articulation
between these two elements. The frontoparietal
suture between the tabs is slightly wavy.
Parietal. The parietal forms the posterior roof
of the skull and is longer and wider than the frontal. It articulates anteriorly with the frontal and
contacts, at its anterolateral margin, the postfrontal (or postorbitofrontal in C. nicterus); the posterolateral margin of the parietal forms the dorsal
margin of the supratemporal fenestra.
A postparietal process of the parietal extends posteriorly along the anterior margin of the supraoccipital transverse crest, overlapping the otooccipital
complex and contacting the supratemporal ventrally. A slender posttemporal fenestra is present in
C. nicterus and N. ablephara, separated at the
midline by a short anterior projection of the supraoccipital and by the short ascending process of the
tectum synoticum (not shown in Figs. 1 and 3), and
delimited anteriorly by the posterior margin of
the parietal (Figs. 1A and 3A). These fenestra are
not present in the two specimens of S. catimbau an-
alyzed, where the posterior margin of the parietal
overlaps the supraoccipital (Fig. 2A). At the posterior
margin of the parietal of N. ablephara and C. nicterus,
a small pit is observed for the anchoring of the
ascending process of the tectum synoticum.
A lateral descending process originates from the
midpoint of the lateral margin of the parietal. In
N. ablephara it is barely noticeable and does not
reach the dorsal tip of the epipterygoid (Figs. 3B
and 6F); in S. catimbau, the process is longer and
is located at the front of the dorsal tip of the
epipterygoid (Figs. 2B and 5D). The highest
degree of development of this process is observed
in C. nicterus, where it completely closes the
lateral wall of the skull from the front of the epipterygoid up to the posterior margin of the orbit
(Figs. 1B and 4F), with a ligamentous connection
to the pterygoid.
Postfrontal. The postfrontal is a short element,
located lateral to the frontoparietal suture. It is
slightly triangular in shape, with short anteromedial and anterolateral ends and a longer posterior
extremity. The postfrontal forms part of the posterodorsal margin of the orbit, contacting the frontal
and parietal dorsally (anterior and posteriorly,
respectively) and the postorbital ventrally. The
bone is not fused in Nothobachia and Scriptosaura
Journal of Morphology
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J.G. ROSCITO AND M.T. RODRIGUES
Fig. 6. N. ablephara, cleared and stained skulls. (A) and (B) Anterior part of the skull in dorsal (A) and ventral (B) views;
anterior to the right. (C) Braincase in medial view; anterior to the left. (D) Braincase in external lateral view; anterior to the right.
(E) Orbital region in lateral view; anterior to the right. (F) Lateral view of the middle part of the skull; anterior to the right. (G)
Articulation between premaxilla and maxilla in lateral view; anterior to the top right. Scale bars from A to F 5 0.5 mm; scale bar
for G 5 0.25 mm.
(Figs. 2A,B and 3A,B); in Calyptommatus, it is
fused to the postorbital.
Postorbital. The postorbital is a long and slender element. It forms a small part of the posterodorsal margin of the orbit, ventral to the postfrontal, and extends posteriorly to meet the squamosal,
with which it forms the inferior bar of the supratemporal fenestra. It contacts the postfrontal anterodorsally and the dorsal surface of the anterior
process of the squamosal posteriorly.
In C. nicterus, a single stout element is
observed, the postorbitofrontal (Figs. 1B and 4E),
corresponding to the embryonic fusion of the postJournal of Morphology
frontal with the postorbital (Roscito and Rodrigues,
unpublished data).
Squamosal. The squamosal is long and slender,
with a sharp anterior process contacting the postorbital (postorbitofrontal in Calyptommatus) and a
ventrally curved posterior process fitting into a
deep notch in the tympanic crest of the quadrate
(Fig. 2B).
Supratemporal. The supratemporal is a small
element, with a wide ventral base and a slightly
sharper dorsal tip, inserted between the squamosal
and the postparietal process of the parietal
(Fig. 1B). Ventrally, it contacts the cephalic con-
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
dyle of the quadrate and the paroccipital process
of the otooccipital.
Vomer. The vomer (Fig. 3C) is the most anterior
component of the skull floor, the palate. It is an
elongated and broad bone situated posterior to the
premaxillary palatal shelf and attached to a cavity
in it (dorsal to the tooth row) through ligaments.
The anterior process of the vomer is sharp but
expands gradually posteriorly, forming a wider
plate that loosely contacts the medial margin of
the maxillary palatal shelf. At the tip of the maxillary teeth row, this plate narrows again to end in
a sharp posterior medial process, overlain medial
and dorsally by the anterior vomerine process of
the palatine. The anterior dorsal surface of the
vomer has a crest that, together with the septomaxilla, encloses the Jacobson’s organ.
Septomaxilla. The septomaxilla is a domeshaped bone, located between the vomer and the
nasal process of the premaxilla (Fig. 2A). It encloses the Jacobson’s organ, protecting it laterally
and dorsally, and the vomer forms the floor to this
capsule. The septomaxilla has a lateral maxillary
process that contacts the maxillary palatal shelf
dorsally; its dorsal surface has an extensive contact with the nasal process of the premaxilla.
Palatine. The palatine forms the middle part of
the skull floor (Fig. 3C). It has an approximately triangular shape, being wider anteriorly. It extends
from the point of the posterior tip of the vomer,
where it contacts the contralateral palatine in the
midline, and narrows and diverges posteriorly to
meet the pterygoid. Anteromedially, its vomerine
process overlaps the posterior end of the vomer;
anterolaterally, the maxillary process overlaps the
posterior end of the maxillary palatal shelf.
Between the medial and lateral extremities of the
anterior margin of the palatine, a broad concavity,
deeper anteriorly and gradually shallower posteriorly, forms the choanal channel.
Posteriorly, the palatine narrows to a pterygoid
process that overlaps the medial palatine process
of the pterygoid. The lateral margin of the palatine
forms the medial margin of the suborbital fenestra.
In C. nicterus, the palatine develops a wide
extension in the middle portion of the bone that
connects to a corresponding expansion of the ectopterygoid and to an anterior extension of the pterygoid to completely close the suborbital fenestra
(Figs. 1C and 4A).
Pterygoid. The pterygoid forms the posterior
portion of the skull floor (Fig. 3C). It is Y-shaped,
with the anterior portion divided into a medial palatine process and a lateral transverse process (pterygoid flange), forming the posterior margin of the
suborbital fenestra, and a long posterior quadrate
process that meets the quadrate. Anteriorly, its palatine process overlaps with the pterygoidal process
of the palatine bone, and its transverse process fits
into a relatively deep facet between the dorsal and
1359
ventral portions of the posteromedial process of the
ectopterygoid. Posteriorly, the quadrate process
extends to meet the medial surface of the mandibular
condyle of the quadrate. The basipterygoid process
contacts the pterygoid at midlength. In C. nicterus,
the anterior portion of the pterygoid is widened to
form a single plate (rather than two separate processes) that participates in the closure of the suborbital
fenestra (Figs. 1C and 4A).
Ectopterygoid. The ectopterygoid is a small
slender bone that forms the external margin of the
suborbital fenestra (Figs. 1C, 2C and 3C). Anteriorly, it contacts the orbital process of the maxilla,
laterally the middle portion of the jugal, and posteriorly the transverse process of the pterygoid,
articulating with the latter through its posteromedial process.
In C. nicterus, the ectopterygoid is wider than
those of N. ablephara and S. catimbau, having a
medial expansion that partially overlaps with the
expansion of the palatine, thereby closing the suborbital fenestra (Figs. 1C and 4A).
Quadrate. The robust quadrate is widely concave medially and can be divided into a mandibular condyle, articulating with the articular in the
mandible, a lateral concave conch with a slight
tympanic crest, and a cephalic condyle articulating
with the supratemporal and paroccipital process;
the ventral tip of the squamosal fits into a deep
notch in the dorsal surface of the conch (Figs. 2B
and 3B).
Epipterygoid. The epipterygoid is a rod-like
element, located between the alar process of the
prootic and the descending process of the parietal
in a vertical position (Fig. 6C). Its ventral tip is
inserted into the dorsal surface of the pterygoid,
and its dorsal tip approaches but does not contact
the descending process of the parietal.
Braincase. The braincase of these three species
is relatively prominent compared with the rest of
the skull, and most of it is exposed behind the parietal. The semicircular canals are easily observed.
In C. nicterus and S. catimbau, a wide occipital
recess (Rieppel, 1985; Figs. 1B, 2B, 4C, and 5E) is
present, whereas in N. ablephara, no such opening
is present (Figs. 3B and 6D).
In N. ablephara and S. catimbau, the bones of
the braincase are fused without visible sutures,
but in C. nicterus, clear sutures can be distinguish
between each bone. Thus, the description of each
element’s limits will be based on the pattern
observed in C. nicterus.
Supraoccipital. The roofs of the braincase and
of the otic capsules are formed by the wide supraoccipital. In N. ablephara and C. nicterus, the short
ascending process of the tectum synoticum, originating at the anterior margin of the supraoccipital,
rests in a shallow pit on the posteroventral margin
of the parietal bone, delimiting two slender posttemporal fenestrae (Figs. 1A and 3A). In none of the
Journal of Morphology
1360
J.G. ROSCITO AND M.T. RODRIGUES
Fig. 7. C. nicterus, mandible in labial (A) and lingual (B)
views. Scale bar 5 1 mm.
S catimbau specimens analyzed was a posttemporal
fenestra present; the anterior margin of the supraoccipital is completely overlapped by the parietal in
this species.
The supraoccipital contacts the dorsal margin of
the prootic anterolaterally and the otooccipital
complex posterolaterally. The posterior margin
forms the dorsal margin of the foramen magnum.
The dorsal ends of the anterior and posterior semicircular canals are joined midlaterally. A transverse crest crosses the dorsal surface of the supraoccipital, extending downward to the paroccipital
process. This crest is much more prominent in N.
ablephara and S. catimbau, whereas in
C. nicterus, it is very faint.
Prootic. The prootic is the anterior component
of the otic capsule. Its anteriorly directed alar process forms part of the lateral wall of the skull, posterior to the eye. In C. nicterus, it expands dorsoventrally to contact part of the descending process
of the parietal dorsally and the epipterygoid ventrally (Fig. 4F). In N. ablephara and S. catimbau,
no ventral extension of this process is found, and
only the most dorsal part approaches the epipterygoid (Figs. 5D and 6D). The anterior ends of the
anterior and horizontal semicircular canals are
located in this area. The incisura prootica, below
the alar process, is an anterior C-shaped exit for
the trigeminal nerve (Fig. 6C). The small facial foramen is observed posteriorly and at the same
level as the trigeminal notch; a crista prootica
begins at the parabasisphenoid and extends up to
this foramen (Fig. 6D). Posterior to the facial foramen is the broad fenestra ovalis (Figs. 4C and 6D),
marking the posterior limit of the prootic. The fenestra ovalis is broader in C. nicterus and smaller
in N. ablephara, with that of S. catimbau of intermediate size. Ventrally, the prootic contacts the
parabasisphenoid anteromedially and the basiocciJournal of Morphology
pital posteromedially; dorsally, it contacts the
supraoccipital.
The internal surface of the prootic can be divided into a dorsal vestibular cavity and a ventral
lagenar cavity (Fig. 6C), both separated by a constriction delimited by the trigeminal notch anteriorly and the fenestra ovalis posteriorly. The ventral margin of the vestibular cavity is pierced by
the anterior and posterior auditory foramina; the
internal opening of the facial foramen is observed
ventral to the anterior auditory foramen.
Columella auris. The columella auris is
inserted into the fenestra ovalis. It is composed of a
broad foot plate, which filles the entire area of the
fenestra, and a shaft projecting laterally. In N. ablephara and S. catimbau, the shaft is relatively long
and slender (Fig. 6D), but in C. nicterus, it is short,
broad, and stout, being nodular and slightly triangular in shape (Fig. 3C). The posterior end of the
cephalic condyle of the quadrate ends proximal to
the shaft of the columella; the paroccipital process
is located dorsal to the fenestra ovalis.
Otooccipital. The compound otooccipital forms
the posterior part of the otic capsule. It is formed by
the embryonic fusion of the opisthotic and
the exoccipital; there is no visible trace of this suture
in C. nicterus. It contacts the supraoccipital dorsally
and the basioccipital ventrally. The horizontal semicircular canal is located above the fenestra ovalis,
and the posterior semicircular canal is located just
anterior to the exoccipital region.
The anterior region of the otooccipital is formed
by the opisthotic, which is wider dorsally and
narrower ventrally. Its anterior margin contacts
the prootic, forming the posterior margin of
the fenestra ovalis, and its anterodorsal margin is
thickened to form the paroccipital process. In
N. ablephara and S. catimbau the process is well
developed, with an anteriorly directed projection
(Fig. 6D), whereas in C. nicterus, this process is
short and does not have this projection (Fig. 4B).
The posterior limit of the opisthotic is determined
Fig. 8. S. catimbau, mandible in labial (A) and lingual (B)
views. Scale bar 5 1 mm.
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
Fig. 9. N. ablephara, mandible. (A) and (B) Labial views.
(C) and (D). Lingual views. Scale bar 5 1 mm.
by the anterior borders of the occipital recess and
of the vagus foramen.
The posterior region of the otooccipital is formed
by the triangular exoccipital, with a wide ventral
base that contributes to the composition of the
occipital condyle and a dorsal end that forms the
lateral margin of the foramen magnum. It forms
the posterior margins of the occipital recess and of
the vagus foramen. N. ablephara does not have an
open occipital recess; this region is covered by a
thin layer of bone (Fig. 6D). However, in S. catimbau and C. nicterus, this opening is quite broad
(Figs. 4B,C and 5E). The foramina for the hypoglossal nerve roots are located in the ventral margin of the exoccipital bone. In N. ablephara, three
small foramina are visible (Fig. 6D), whereas in S.
catimbau and C. nicterus, only two small foramina
are present (Figs. 1B and 2B).
Basioccipital. The basioccipital forms most of
the braincase floor, from the parabasisphenoid to the
occipital condyle. It is a concave plate, slightly pentagonal in shape, fusing anteriorly to the parabasisphenoid and contacting laterally the prootic (anterior) and the otooccipital (posterior) (Figs. 1C, 2C
and 3C). It has a minor contribution to the ventral
margin of the occipital recess.
Parabasisphenoid. The compound parabasisphenoid is composed of the endochondral basisphenoid, which ossifies from the embryonic acrochordal
cartilage, the basipterygoid processes, and the dermal parasphenoid, which forms in later stages of
1361
development around the basisphenoid. This parabasisphenoid is formed by an anteriorly directed
rostral process, which is long and slender in
N. ablephara (Fig. 3C) and short and stout in
C. nicterus (Fig. 1C), with that of S. catimbau (Fig.
2C) of an intermediate stage. It contacts the prootic
posterolaterally and is fused to the basioccipital
posteriorly. The basipterygoid process projects anterolaterally to meet the pterygoid medially.
Orbitosphenoid. The paired small orbitosphenoids are located anteriorly with respect to the
braincase elements and internally with respect to
the orbits, at an angle to the dorsoventral axis of
the skull. It is a relatively thin bone with a triangular shape, connecting to the interorbital cartilages (Figs. 3B and 5F).
Mandible. The mandible is similar in the
three species (Figs. 7–9). Meckel’s cartilage runs
through Meckel’s canal, from the most anterior
tip of the dentary posterior to the adductor fossa.
A relatively short retroarticular process is present, as well as a short coronoid process. The convex splenial shapes the inferior border of the
mandible.
Dentary. The anterior part of the mandible is
formed by the dentary, the largest bone in the jaw.
The posterior end of the bone, at the labial surface,
contacts the splenial and angular ventrally and
the surangular posteriorly and underlies the anterior directed labial process of the coronoid dorsally.
In C. nicterus and S. catimbau, this process
extends over the posterior margin of the dentary
up to the level of the last (posterior) tooth (Figs.
7A and 8A), whereas in N. ablephara, it extends
even further (Fig. 9A,B). At the lingual surface,
the opening of Meckel’s canal is observed at the
anterior end of the dentary, and Meckel’s cartilage
extends up to this opening. The posterior margin
of the bone is overlapped by the splenial ventrally
and by the anteromedial process of the coronoid
(Fig. 9C,D). The alveolar portion of the dentary of
Fig. 10. S. catimbau, hyoid apparatus in ventral view; (A)
Cleared and stained specimen, (B) drawing of A. In both figures,
anterior is to the top of the image. Scale bar in A 5 0.5 mm.
Journal of Morphology
1362
J.G. ROSCITO AND M.T. RODRIGUES
N. ablephara and S. catimbau bears 15 unicuspid
teeth (Figs. 8A and 9A), whereas in C. nicterus,
only 12 teeth are present (Fig. 7B).
Coronoid. The coronoid is triangular with a
short dorsal coronoid process. The labial process,
relatively thin in C. nicterus and S. catimbau but
longer and stouter in N. ablephara, is directed
anteriorly and overlaps the posterior dorsal end of
the dentary. On the lingual surface of the mandible, the anteromedial process overlaps the dentary
and contacts the splenial ventrally, and the prearticular and surangular posteriorly. In C. nicterus,
this process is short and broad, with its ventral
margin overlapped by the splenial (Fig. 7B).
In N. ablephara and S. catimbau, this process is
more elongate anteriorly, being wider in the former and slender in the later, but is again overlapped by the splenial extending up to the level of
its alveolar foramen (Figs. 8B and 9C,D). The slender posteromedial process of the coronoid overlaps
the prearticular, forming the anterior margin of
the adductor fossa.
Splenial. The splenial (Fig. 9C,D) is a robust
bone that forms the midventral portion of the lingual surface of the mandible. It overlaps the dentary anteriorly and the anteromedial process of
the coronoid dorsally, and it contacts the prearticular posterodorsally and the angular posteroventrally. The ventral margin of the bone is convex
and shapes the inferior margin of the mandible.
Two foramina are present: a large alveolar foramen at the anteromedial portion of the splenial
and a smaller anterior mylohyoid foramen ventral
to the former. The ventral margin of the splenial is
found on the labial surface of the mandible, ventral to the dentary.
Angular. The small angular is located on the
ventral margin of the mandible, posterior to the
splenial. It is more exposed on the labial surface,
contacting the surangular posterodorsally and having its anterior end overlapped by the dentary
(Fig. 8A). On the lingual surface, only a strip of
bone is seen. This lies ventral to the posterior end
of the splenial, is overlapped by it anteriorly, and
contacts the prearticular posteriorly (Fig. 8B). The
posterior mylohyoid foramen is visible ventrally.
Surangular. The surangular is a large and
stout bone that forms the posterior portion of the
labial surface of the mandible, posterior to the
dentary (Fig. 9). It contacts the coronoid anterodorsally, the dentary anteriorly, and the angular
ventrally and forms the external margin of the
adductor fossa. A large surangular foramen is
observed next to the contact with the coronoid.
Posterior to this foramen, another small foramen
opens internally next to the anterior part of the
prearticular. Posteriorly, the surangular is fused
with the prearticular-articular complex.
Prearticular-articular complex. This complex
is formed by the fusion of a large prearticular, formJournal of Morphology
ing most of the posterior end of the lingual surface
of the mandible, with the small articular, which provides the articulation to the skull on its dorsal surface (Fig. 9C,D). The prearticular forms the floor
and the internal margin of the adductor fossa, while
the articular forms its posterior margin. The retroarticular process is formed by the fused surangular
and prearticular-articular complex.
Hyoid apparatus. The hyoid apparatus (Fig. 10)
is a complex of skeletal elements located ventral to
the mandible, in the throat region, and supports the
muscles associated with this region. The hyoid apparatuses of the three species are similar to each other,
thus the description given here applies to all three
species.
It is composed of a short triradiate basihyal, a
long glossohyal (lingual process) extending up to
the mandibular symphisis, and three pairs of visceral arches (Fig. 10B). The first visceral arch, the
hyoid cornu, originates from the anterior border of
the basihyal and is directed anteriorly. From its
mid portion originates a posteriorly directed process, the epihyal. The second visceral arch corresponds to the first ceratobranchial, connected to
each posterior end of the basihyal and extending
posteriorly to connect to the first epibranchial. The
third visceral arch corresponds to the rudimentary
second ceratobranchial. It is thin and short, and is
located between the first ceratobranchial and the
basihyal. The second epibranchial (Fig. 10A) is a
free sigmoidal element, orientated lateroposteriorly
and located anterior to the first ceratobranchial and
dorsal to the epihyal; its anterior end is curved to
approach the ventral portion of the otooccipital.
The first ceratobranchial is the only ossified element of the hyoid apparatus. All other elements consist of calcified cartilage in the adult, except for the
free second epibranchial which remains cartilaginous.
DISCUSSION
The skeleton is intimately associated with life
habits and reflects functional adaptations to the
style of living. The evolutionary transition from
quadrupedal to a snake-like body plan and fossorial
and burrowing locomotion requires the evolution of
a complex of skeletal adaptations (Hanken and
Wake, 1993; Lee, 1998; Rieppel, 1984, 1996). The
consequences for skull morphology in fossorial animals are intimately associated with miniaturization
and with the development of a solid skeletal covering for the brain and sense organs, protecting them
from the impacts of the subterranean limbless locomotion (Rieppel, 1984). Thus, the reduction of body
diameter and loss of a neck region (with the uniformization of the body and head diameter), the relative increase in braincase size, the increase of skull
stoutness with loss of skull fenestrae, closure of
the lateral walls, and more complex connections
between the bone elements, especially due to the
CRANIAL OSTEOLOGY OF FOSSORIAL GYMNOPHTHALMIDS
utilization of the skull as a burrowing tool (Camp,
1923; Gans, 1960, 1969; Lee, 1998; Rieppel, 1984,
1996; Wake, 1993) are frequent and convergent evolutionary events. Therefore, fossoriality requires
akinetic and robust skulls that protect the brain
and sensorial organs from the mechanical forces of
burrowing (Rieppel, 1996).
Several features of the skull morphologies of
C. nicterus, N. ablephara, and S. catimbau are
clearly related to the adaptations to the fossorial
and burrowing life style but reflect morphological
adaptations to different levels of fossoriality. The
skulls are stout and rigid as a result of strong and
elaborated articulations and overlap between elements. The degree of fossoriality can be inferred
through an analysis of the connections between
skull elements: stronger and more complex articulations render a strengthened skull that is capable
of supporting a greater stress. In contrast, weaker
articulations reflect weaker evolutionary pressures
for protection of the brain. Also, some bones show
increased growth to contact neighboring elements
and close open spaces in the skull, offering further
protection to the brain and sense organs from the
physical impacts to which the head is subjected.
The sharp and projecting snout is formed by the
thick horizontal plate of the premaxilla, which
forms a strong articulation with the maxilla (in
C. nicterus and S. catimbau), and, together with
the large nasal process, builds a tool for burrowing. However, in N. ablephara, the articulation
between the premaxilla and maxilla is weaker,
probably indicating a lesser degree of stress to
which the skull is subjected. In the fossorial limbless gymnophthalmid Bachia bicolor (Tarazona
et al., 2008), the articulation between premaxilla
and maxilla is similar to that observed in N. ablephara, while in Vanzosaura rubricauda (Guerra
and Montero, 2009), their close relative, there is
no contact between these elements.
The frontoparietal contact is tightened through
the well-developed frontoparietal tabs and a complex interlocked suture, thus excluding any possibility of cranial mesokinesis (Lee, 1998; Metzger,
2002; Rieppel, 1984, 1996). Also, the loss of the
posttemporal fenestrae in S. catimbau indicates an
akinetic and rigid skull due to the overlap of the
supraoccipital by the parietal (Bell et al., 2003;
Evans, 2003; Metzger, 2002; Müller, 2002).
The reduced orbit and nasal openings in this fossorial lineage result in wider bones composing the
anterior dorsal roof and lateral wall of the snout.
The most extreme case of this morphological
arrangement is observed in C. nicterus, followed
by S. catimbau and by N. ablephara.
The well-developed cristae cranii of the frontal
of C. nicterus encapsulate the nasal bulbs and establish strong contacts with neighboring bones
such as the palatine and prefrontal. Also, the
extreme growth of the ventral process of the parie-
1363
tal and of the alar process of the prootic results in
a completely closed posterior lateral wall of the
skull in C. nicterus. In addition, the growth of
bony extensions of the ectopterygoid, pterygoid,
and palatine, which contact and overlap each
other, in association with the maxillary palatal
shelf, completely closes the suborbital fenestra.
Together with a near contact between the maxillary palatal shelf and the vomer, this forms a rigid
palate, suggesting a greater degree of adaptation
to fossoriality in this species. These peramorphic
traits (Rieppel, 1996) offer a higher degree of protection for the brain and contrast to the condition
observed in the other two species. These traits
evolved convergently in other head-first burrowers
(Lee, 1998; Rieppel, 1996; Savitzky, 1983; Tarazona et al., 2008), although the different degrees of
morphological differentiation suggest different degrees
of adaptation to fossoriality.
The enlarged otico-occipital region in relation to
the dermatocranium results in a shifting in the
position of the supraoccipital to directly contact
the posterior margin of the parietal. As a consequence, the posttemporal fenestra is closed or
reduced in size. The closure of the posttemporal
fenestrae is also observed in other serpentiform or
miniaturized (Hanken and Wake, 1993) squamates, such as some species of Scincidae, Amphisbaenia, Dibamidae, Serpentes, and Pygopodidae
(Lee, 1998; Montero and Gans, 1999; Rieppel,
1981, 1984, 1996; Tarazona et al., 2008). As revised by Rieppel (1984), this relative increase in
braincase size observed in small skulls is a consequence of the development of functional semicircular canals, whose curvatures requires a certain
minimum radius for proper efficiency.
The triradiate jugal of C. nicterus, with a welldeveloped free posterior process, is unique among
Gymnophthalmidae, in which the jugal is always
semilunar in shape. A free posterior jugal process
is also observed in some lacertids, scincids and
agamids (Evans, 2008), but it never develops to
such large size as found in Calyptommatus. In
Sphenodon, the large posterior process of the jugal
forms, together with the small quadratojugal, a
complete lower temporal bar. The presence of a
posterior process of the jugal is now considered a
secondary, because in basal lepidosaurians, no
such process was present and, hence, no lower
temporal bar (Evans, 2003; Müller, 2003). The development of such process in C. nicterus may be a
consequence of the peramorphic development of
some of the skull elements, such as the ventral
process of the parietal or the growth of the bony
extensions of the palate elements. Further study is
needed to investigate if the presence of this process has a functional significance in feeding forces.
A commonly observed pattern in fossorial morphologies is the reduction/loss of elements and/or
simplification of their morphology (Hanken and
Journal of Morphology
1364
J.G. ROSCITO AND M.T. RODRIGUES
Wake, 1993). The skull of miniaturized animals
may lack bones that are present in related and
nonminiaturized species or show poor development
of other elements. This aspect is observed in the
reduced number of teeth in the premaxilla, maxilla, and dentary, with the highest degree of reduction being observed in C. nicterus, a feature also
seen in miniaturized salamanders (Hanken and
Wake, 1993).
The poor development of the shaft of the columella as well as that of the paroccipital process in
C. nicterus in comparison with those of N. ablephara and S. catimbau and the absence of an
ascending process of the tectum synoticum and of
posttemporal fenestrae in S. catimbau are features
associated with the enlargement of the otic capsule. The increase in size of otic capsule imposes
physical limitations on the size and development
of other structures, such as observed by Rieppel
(1984) for Dibamus species, Lee (1998) for several
species of dibamids, snakes, and amphisbaenians,
Müller (2002) for Parvilacerta parva, and Tarazona et al. (2008) for B. bicolor and others.
Fusion of elements is frequent as a consequence
of structural simplification (Lee, 1998). The absence of a lacrimal may indicate either the loss of
this element or its fusion with the prefrontal; the
analysis of embryonic development of this region
may elucidate the condition observed in adult
forms. Also, the size of the lacrimal flange (larger
in N. ablephara and S. catimbau and absent in C.
nicterus) and the presence of a single element representing the fusion of the postorbital with the
postfrontal in C. nicterus (while in N. ablephara
and S. catimbau both bones are distinct) indicate a
greater degree of structural reduction in specific
regions of the skull of C. nicterus. The presence of
a single element in the postorbital region is frequently observed in species from several taxa
(Camp, 1923). Nevertheless, although fossoriality
has evolved repeatedly in Gymnophthalmidae, the
only other genus presenting this condition is Alopoglossus, as well as the species Dryadosaura nordestina, Anotosaura vanzolinia and Colobosauroides cearensis (Evans, 2008, Rodrigues et al.,
2005, 2009). Evans (2008) also reported a postorbitofrontal in Heterodactylus following Presch (1980);
this is in contrast to our observations in cleared and
stained specimens of H. lundii and H. imbricatus,
which have distinct postorbital and postfrontal s.
The identification of the postorbitofrontal is quite
variable, being represented by either the postorbital
or postfrontal alone or by a fusion of both (Camp,
1923). In C. nicterus, the postorbitofrontal is represented by the fusion of the well-developed postorbital
with a reduced postfrontal; both elements are clearly
identified in late embryonic stages (Roscito and
Rodrigues, unpublished data).
C. nicterus is also peculiar in having welldefined sutures between the braincase elements as
Journal of Morphology
an adult, whereas in its closest relatives N. ablephara and S. catimbau, no sutures are observed.
The former pattern agrees with that observed in
the gymnophthalmid B. bicolor (Tarazona et al.,
2008), but the absence of sutures in adults seems
to be more common, e.g., in the gymnophthalmids
Euspondylus acutirostris (Montero et al., 2002),
Potamites ecpleopus (Bell et al., 2003), Dryadosaura
nordestina (Rodrigues et al., 2005), Caparaonia
itaiquara, Brazil (Rodrigues et al., 2009), Alexandresaurus camacan (Rodrigues et al., 2007), and
V. rubricauda (Guerra and Montero, 2009).
The presence of a large occipital recess in C. nicterus and S. catimbau contrasts with the completely closed occipital recess in N. ablephara.
Although it might be consequence of the small
skull adapted to burrowing habits, the closure of
the occipital recess is found in many different species and is not always correlated with fossoriality
(Rieppel, 1985). However, an open occipital recess
is also characteristic of fossorial pygopodids, such
as Aprasia and Pletholax (Rieppel, 1985) and
of fossorial scincids (Haas, 1936; Greer, 2002;
Rieppel, 1985). According to Rieppel (1985), lizards
that show a closed occipital recess lack an external
tympanic membrane and have a large stapedial
footplate, all related structural modifications for
the transmission of ground pressure waves rather
than airbone vibrations. This is not the case in
N. ablephara, which shows a smaller stapedial footplate compared with C. nicterus and S. catimbau.
Therefore, the skull of fossorial and burrowing
lizards is a complex set of structural modifications
related to cranial consolidation and, also of autapomorphic features. The evolution of head-first burrowing and the structural modifications associated
with it are convergent features, which, in the
Gymnophthalmidae, evolved several times independently (Pellegrino et al., 2001). A complete
study of the development of such features, comparing the patterns observed in distantly related species, will probably provide an important evolutionary scenario for their history and may also shed
light on the morphological transformations associated with the origin of snakes, as discussed by
Rieppel (1984, 1996).
ACKNOWLEDGMENTS
The authors thank Hussam Zaher and Carolina
Castro-Mello, from Museu de Zoologia da Universidade de São Paulo (MZUSP), for access to the
stained specimens.
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