Morphology and intraspecific variation in the skull and mandible of the slider turtle Trachemys dorbigni (Testudines, Emydidae)

Abstract

Testudines generally presents a considerable wealth of osteological elements of the skull that makes crucial the detailed knowledge of these bone structures, mainly in solving problems of classification and determination of species. Emydidae is an important group of chelonians, but the cranial anatomy knowledge is limited, mainly of the species of the genus Trachemys. The aim of the present study is to describe the osteology (in particular, the intraspecific variations) of the skull and mandible of T. dorbigni. 82 specimens of T. dorbigni from the Herpetological Collection of the Laboratory of Vertebrate Zoology/Institute of Biology/Universidade Federal de Pelotas were used in this study. The results indicated a set of characteristics not previously described for the specie’s skull, as well as several characteristics intraspecifically variable. Intraspecific variation was found in the pattern of jugal, frontal, prefrontal, vomer, quadratojugal and exoccipital bones, further the cases of absence and diversification in the position of the foramina praepalatinum and foramen nervi hypoglossi, and an observation of foramens that were not described in literature. Therefore, it is possible to state that there is considerable intraspecific variation in the Trachemys dorbigni’s skull, although it maintains general characteristics similar to other Emydidae’s species.

Full text

Vol.:(0123456789)
1 3
Zoomorphology
https://doi.org/10.1007/s00435-020-00491-4
ORIGINAL PAPER
Morphology andintraspecic variation intheskull andmandible
oftheslider turtle Trachemys dorbigni (Testudines, Emydidae)
PriscilaRockenbachPortela1 · RógerJeanOliveira1· FabioPereiraMachado1· CésarJaegerDrehmer1·
AnaLuísaSchinoValente2· JoséEduardoFigueiredoDornelles1
Received: 24 December 2019 / Revised: 15 May 2020 / Accepted: 18 May 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract
Testudines generally presents a considerable wealth of osteological elements of the skull that makes crucial the detailed
knowledge of these bone structures, mainly in solving problems of classification and determination of species. Emydidae is an
important group of chelonians, but the cranial anatomy knowledge is limited, mainly of the species of the genus Trachemys.
The aim of the present study is to describe the osteology (in particular, the intraspecific variations) of the skull and mandible
of T. dorbigni. 82 specimens of T. dorbigni from the Herpetological Collection of the Laboratory of Vertebrate Zoology/
Institute of Biology/Universidade Federal de Pelotas were used in this study. The results indicated a set of characteristics
not previously described for the specie’s skull, as well as several characteristics intraspecifically variable. Intraspecific vari-
ation was found in the pattern of jugal, frontal, prefrontal, vomer, quadratojugal and exoccipital bones, further the cases of
absence and diversification in the position of the foramina praepalatinum and foramen nervi hypoglossi, and an observation
of foramens that were not described in literature. Therefore, it is possible to state that there is considerable intraspecific vari-
ation in the Trachemys dorbigni’s skull, although it maintains general characteristics similar to other Emydidae’s species.
Keywords Osteology· Cranium· Intraspecific variation· Turtle· Cryptodira
Introduction
Trachemys dorbigni is a semi-aquatic freshwater turtle with
natural distribution in southern Brazil, in Uruguay and
northern Argentina (Alcade etal. 2012). This turtle belongs
to the suborder Cryptodyra (referring to the turtles that
retract the neck into the carapace in a vertical plane) and
family Emydidae, an important group within the chelonians,
containing around 50 living species (Rodhin etal. 2010).
Studies that are concerned with describing the osteol-
ogy of living chelonians are rare and those that have been
published are often not very detailed. Most published stud-
ies focus on morphological differences between species or
between groups of higher taxonomic categories (Gaffney
1972, 1977; Jones et al. 2012), and studies that evaluate
detailed skull osteology and intraspecific variations (which
are usually discrete but relevant variations) are scarce.
The following papers are concerned with the description
of turtle skulls and provide important information about the
morphology of these species: Trionyx gangeticus Cuvier,
1825, Chelydra serpentina (Linnaeus, 1758), Podocnemis
expansa (Schweigger, 1812), Emydura macquarrii Iverson
1992, Pseudemydura umbrina Siebenrock, 1901, Plate-
mys (Chelonia spp.), Chrysomnia spp. (Schneider, 1792),
Phrynops geoffroanus (Schweigger, 1812), Hydromedusa
tectifera Cope, 1869, Phrynops gibba Gaffney, 1977, Chelo-
dina expansa Gray, 1857, Chelus fimbriatus (Carnea etal.,
2011), Caretta caretta (Linneaus, 1758), and Lepidochelys
kempii (Garman, 1880) (Gaffney 1972, 1977; Jones etal.
2012; Mansharamani 1965; Romão and Santos 2014).
Despite the relatively low number of publications of oste-
ology of living testudines, much of what is known about the
group’s cranial osteology in general is due to the effort of
paleontologists in describing fossil species. The extremely
rich fossil record of turtles favors to trace the evolutionary
history in a very robust way through the morphological data
provided by osteological descriptions and phylogenies based
* Priscila Rockenbach Portela
priscila.rportela@gmail.com
1 Departamento de Ecologia, Zoologia e Genética,
Universidade Federal de Pelotas, Pelotas, RS, Brazil
2 Departamento de Morfologia, Universidade Federal de
Pelotas, Pelotas, RS, Brazil

Zoomorphology
1 3
on morphological characters (Gaffney etal. 2007; Joyce and
Bell 2004; Joyce 2007).
For this reason, much of the detailed data of testudines
cranial morphology is described in phylogeny articles
(Gaffney etal. 2007; Joyce and Bell 2004; Joyce 2007).
Thus, probably the main application of testudines morpho-
logical data is to provide more information to help elucidate
the evolutionary history of turtles and phylogenetic relation-
ships, between fossils and living groups.
The complete osteology (skull and postcranium) of T.
dorbigni was described by Souza etal. (2000), who pre-
sented data on the position of bones, sutures and the occur-
rence of some foramina. However, the aim of this paper
was to provide a generalist description and did not concern
to elucidate osteological details of the sincraniun, such
as notches, bone features, occurrence of some foramina,
description of some bones contacts, as well as details of
intraspecific variations and key features that vary between
sexes (Souza etal. 2000).
In addition, there is no record in the literature of skull
characters with phylogenetic importance, which are com-
monly adopted to review the evolutionary relationships
of fossil and extant testudines. In other words, there is an
absence of data that allows a morphological comparison
between T. dorbigni and others quelonian species.
Thus, the aim of this paper is to describe the osteology of
the skull and mandible of T. dorbigni including osteological
features not described for the species, and also to identify
and describe intraspecific variations and verify the occur-
rence of sexual dimorphism in these features.
Materials andmethods
We used 83 skulls and jaws of T. dorbigni specimens (37
females, 24 males and 22 undetermined), held by the Herpe-
tological Collection of the Vertebrate Zoology Laboratory of
the Universidade Federal de Pelotas, all of which originated
from the south of the state of Rio Grande do Sul.
The osteological features were observed macroscopically
and under a stereoscopic microscope and described by the
dorsal, lateral, ventral and posterior views (for the skull), and
medial and lateral views of the mandible. The osteological
nomenclature used followed Gaffney (1972, 1979).
Results
Skull osteology
In the dorsal view, the dermocranial surface of the skull
of T. dorbigni contains the prefrontal, frontal, postorbital,
parietal, jugal, quadratojugal and squamosal bones (Fig.1a).
The floor of the fossa temporalis superior is formed by
the prootic, parietal, squamosal, quadrate, opisthotic and
supraoccipital bones, the latter of which also forms the crista
supraoccipitalis. Important structures are present in the dor-
sal view, including the fossa orbitalis, the fossa temporalis
superior, and the crista supraoccipitalis.
Ventrally, the skull has different planes and several bones.
The rostrum is composed of the premaxilla, maxilla, vomer,
and palatine bones (Fig.1b). Through the fossa temporalis
inferior, it is possible to see the inner portion of the maxilla,
parietal, pterygoid and quadratojugal bones. In the most dor-
sal plane of the ventral view, posterior to the rostrum bones,
large parts of the pterygoid, basisphenoid and basioccipital
bones are visible. The caudal portion of the skull is formed
by part of the quadrate and its mandibular condyles, by the
squamosal, opisthotic, and exoccipital bones, and by the
final portion of the crista supraoccipitalis.
In the lateral view of the skull of T. dorbigni, the prefron-
tal, frontal, maxilla, jugal, postorbital, quadratojugal, quad-
rate, parietal and supraoccipital bones are visible (Fig.1c).
From this view, it is possible to see the fossa orbitalis, as
well as all the surrounding bones. This is also the only
view that allows ample visualization of the cheek emar-
gination and tympanic cavity (constituted by the quadrate
bone). The caudal view of the skull shows different levels
of depth. The bones in the most anterior plane are the squa-
mous, opisthotic, supraoccipital, and exoccipital, as well as
the structures of the occipital condyle and the large foramen
magnum (Fig.1d).
Prefrontal
The prefrontals composed of a pair of bones separated by a
mesial suture, located in the anterior portion of the rostrum
in the dorsal view. The bone contributes to a large part of
the anterior rostrum outline, delineating the dorsal margin
of the fossa nasalis and the anterodorsal orbital rim. This
interorbital area, filled by the dorsal prefrontal plate, has a
smooth surface and it is free from any prominence.
The prefrontal lateral margin articulates briefly with the
maxilla between the fossa nasalis and fossa orbitalis. A brief
process extends posteriorly from the prefrontal, towards the
frontal, articulating to this bone in a V-shaped suture. In
some specimens, this suture may have a smaller angulation,
resembling an “L” shape, and consequently, the prefrontal
advances slightly dorsally, reaching the posterior portion of
the postorbital bone (Fig.3b). In these cases, the prefrontal
participation in anterodorsal margin of the orbit becomes
much larger. Some specimens may exhibit this configuration
asymmetrically in the prefrontal posterior portion (Fig.2a).
Part of the prefrontal is seen through the nasal opening,
forming the anterior border of the foramen interorbitale
and the anterodorsal margin of the foramen orbito-nasale.

Zoomorphology
1 3
The anterior wall of the orbits is formed by a descending
process of the prefrontal, which contacts the palatines and
vomer.
Frontal
Pair of bones articulated by a mesial suture. The frontal larg-
est surface is present in the dorsal view, where it is articu-
lated posteriorly with the prefrontal by an angular V-shaped
or, in some specimens, a less angular L-shaped suture
(Fig.2). The specimens with a prefrontal–frontal–angular
suture (V-shaped), have an anterolateral process that forms
a small part of the dorsal margin of the orbit (Fig.2). Lat-
erally, the frontal is articulated with the postorbital and
posteriorly with the parietal, which presents a characteristi-
cally delineated suture in a small “V” shape, exactly at its
midpoint. This characteristic is an effect of the emission of
two brief posterior processes (one lateral and one medial)
towards the parietal.
Parietal
Composed of a pair of bones articulated together by a mesial
suture. The anterior portion articulates with the frontal and
the lateral portion articulates with the postorbital. Posteri-
orly, the parietal gradually narrows and emits a conspicu-
ous acuminate process that forms the anterior portion of the
crista supraoccipitalis. The parietal bone has a brief articu-
lation with the supraoccipital bone, characterized by a “V”
shaped suture above the crest.
The portion of the parietal in the floor of the fossa tem-
poralis superior makes lateral contact with the prootic and
may present a convex deviation towards the interior surface
of this bone. Posteriorly, in addition to the supraoccipital
articulation, the parietal also articulates laterally with the
opisthotic.
The parietal emits a descending process that forms the
lateral braincase wall where the trigeminal foramen is
located. This process contacts the pterygoid, palatine, and
prootic bones.
Postorbital
This bone forms most of the orbital posterodorsal margin.
There is a process that runs in a posterolateral direction
through the anterior border of the fossa temporalis inferior
(characterized by a “U” shape). In the posterior portion of
this dorsolateral process, the postorbital bone articulates
Fig. 1 Illustration of Trachemys
dorbigni skull from: a dorsal, b
ventral, c lateral and d posterior
view. Prefrontal (pf), frontal
(fr), postorbital (po), parietal
(pa), jugal (ju), maxilla (mx),
premaxilla (pm), pterygoid (pt),
quadrate (qu), quadratojugal
(qj), squamosal (sq), supraoc-
cipital (so), opisthotic, (op),
prootic (pr), exoccipital (ex),
basisphenoid (bs), basioccipital
(bo). Author’s drawing

Zoomorphology
1 3
with quadratojugal, except in the specimens where the
anterolateral process of the squamosal goes over the quad-
ratojugal and touches the postorbital bone. The dorsal por-
tion of the postorbital articulates entirely with the jugal
and in some specimens, may slightly touch the maxilla at
the fossa orbitalis line (Fig.3).
Quadratojugal
Pair of bones located in the lateral portion of the skull, ante-
rior to the quadrate and posterior to the jugal and postorbital.
In some specimens, the quadratojugal extends dorsally to
form a small part of the lateral margin of the fossa tempora-
lis superior. In others specimens, in place of this projection,
there is an articulation between the squamosal and the jugal,
both of which articulate dorsally with the quadratojugal.
There is also a small foramen (innominate) in the center of
the bone (Fig.4).
Quadrate
Pair of bones located laterally in the skull of T. dorbigni,
which have a very irregular shape and important bone fea-
tures, such as the tympanic cavity, the articular process, and
the mandibular condyle (Fig.5). The tympanic cavity is a
large circular concavity formed by the quadrate. There is a
notch in the central portion of the tympanic cavity, the colu-
mella auris, and another, the antrum postoticum, in the dor-
sal portion, fully surrounded by the quadrate. The articular
process articulates with the area articularis mandibularis.
The quadrate is present in the floor of the fossa tempora-
lis superior and forms its lateral walls. In the dorsal view,
the quadrate articulates medially with the opisthotic. In the
ventral view, its medial articulation is principally with the
pterygoid, and its caudal portion, which is in a triangular
Fig. 2 Dorsal view of Trachemys dorbigni rostrum (CHR-171) show-
ing prefrontal with posterior border in “L” shape (a) and asymmetri-
cal design of Trachemys dorbigni (CHR-169) rostrum (b). Suture
between prefrontal and frontal (black arrow); suture between prefron-
tal and postorbital (yellow arrow); frontal (fr); maxilla (mx); parietal
(pa); premaxilla (pm); postorbital (po); prefrontal (pf)
Fig. 3 Right side of Trachemys dorbigni (CHR-111) skull by dorsal
view. Floor of the fossa temporalis superior (dashed line); condylus
occipitalis (co); frontal (fr); jugal (ju); opisthotic (op); parietal (pa);
prefrontal (pf); postorbital (po); prootic (pr); pterygoid (pt); quadrate
(qu); quadratojugal (qj); supraoccipital (so); squamosal (sq)
Fig. 4 Lateral detail of the skull of Trachemys dorbigni (CHR-111).
Quadratojugal foramen (arrow); cheek emargination (dashed line);
jugal (ju); maxilla (mx); parietal (pa); postorbital (po); pterygoid (pt);
quadrate (qu); quadratojugal (qj); supraoccipital (so)

Zoomorphology
1 3
shape, articulates with the opisthotic (medial) and the squa-
mosal (lateral).
Jugal
Paired bone located ventrally to the postorbital and anterior
to the quadratojugal. In some specimens, its anterior margin
forms part of the posterior margin of the orbit, and in oth-
ers specimens, the anterior border is limited dorsally by the
postorbital and ventrally by the maxilla, allowing a short
articulation between both bones (Fig.6). This variation can
also occur in a bilaterally asymmetric way, such that on one
side of the skull, the jugal forms the margin of the orbit, and
on the other side does not (Fig.7a, b). The jugal also make
up the anterior outline of the cheek emargination.
Pterygoid
Paired bone, composing a large central extension of the
neurocranial floor. The pair is separated by a mesial suture
from the anterior border to approximately its middle course,
where it diverges and laterally surrounds the basisphenoid
and basioccipital. Anteriorly, the bone articulates with the
Fig. 5 Skull of Trachemys dorbigni (CHR-144) in the lateral view
showing the quadrate with associated bones. Cavum tympani (dashed
line); condylus mandibularis (1); processus articularis (2); columella
auris (3); incisura columelae auris with a posterior opening (4);
antrum postoticum (5); quadratojugal (qj); squamosal (sq)
Fig. 6 Lateral view of the ros-
trum of the skull of Trachemys
dorbigni. Specimen (CHR-154)
with the jugal isolated from the
orbital border by the articulation
between postorbital and maxilla
(a). Specimen (CHR-101) with
the jugal bone forming the
posterior orbital border (b).
Dermocranial surface of the
jugal bone (dashed line); jugal
(ju); maxilla (mx); quadratoju-
gal (qj); parietal (pa); postorbi-
tal (po); pterygoid (pt)
Fig. 7 Rostral portion of Tra-
chemys dorbigni skull (CHR-
103) from lateral view showing
asymmetry of the jugal. Right
(a) and left side (b). Dermocra-
nial surface of the jugal (dashed
line); jugal (ju); maxilla (mx);
quadratojugal (qj); parietal (pa);
postorbital (po); pterygoid (pt)

Zoomorphology
1 3
jugal, palatine, vomer and delimits the foramen palatinum
posterius. Laterally, the pterygoid makes up the medial walls
of the fossa temporalis inferior, presents a conspicuous
curved process called the processus pterygoideus externus
and also articulates briefly with the quadrate bone.
Pterygoids also present a posterior elongation that forms
the flooring of the cavum acustico-jugulare.
Opisthotic
Paired bone, with a subtriangular shape in dorsal view,
located in the posterior portion of the skull and in the floor
of the fossa temporalis superior. Dorsally, its thin portion
(anterior) articulates with the parietal, medially it articulates
with the supraoccipital and laterally with the squamosal. In
the posterior view, the opisthotic is located laterally to the
exoccipitals and forms the ceiling of the fenestra postotica.
Basioccipital
A single bone in the posteromedial portion of the skull, as
observed from the palatal view. Anteriorly it contacts with
the basisphenoid and laterally with the pterygoids. The bone
projects posteriorly, forming the occipital condyle. Ventral
to the condyles, there is a pair of small processes on the
surface of the basisphenoid, called the tuberculum basioc-
cipitale (Fig.8b). In the posterior view, the occipital condyle
(formed by the basioccipital) is located between the pair of
exoccipital bones.
Basisphenoid
Single bone, with a triangular outline. The anterior vertex
is opposite to a dorsal line suture, which is articulated with
the basioccipital bone. Its ventral surface is totally sur-
rounded by the pterygoids (laterally) and by the basioccipital
(posteriorly).
Exoccipital
A pair of bones, lateral to the basioccipital, posterior to the
fenestra postotica and medial to the opisthotic. The exoccipi-
tals bones form the lateral frame of the foramen magnum. In
this bone, on each side of the occipital condyle, are the pairs
of foramina nervi hypoglossi and more laterally the large
forame jugulare posterius (Fig.8a). In some specimens, a
small foramen may be found between the foramina nervi
hypoglossi (fnh) and the foramen jugulare posterius (p)
(Fig.8b).
Maxilla
Paired bones with an elongated shape, located in the antero-
lateral portion of the rostrum. They constitute almost all the
anterior outline of the skull and form the ventral boundary
as well as the floor of the fossa orbitalis. The posterior por-
tion of the maxilla has a dorsal process (between the fossa
orbitalis and apertura narium externa), that contacts the
prefrontal bone, and this process forms part of the lateral
margin of the apertura narium externa. The posterior por-
tion of the maxilla articulates dorsally with the jugal and, in
some specimens, with the postorbital from the lateral view.
In palatal view, a posterior part of the maxilla articulates
from the center to the sides, with vomer, palatine and jugal.
The maxillas have a strongly trabeculated bone surface due
to the insertion of the horny beak in this region.
Premaxilla
A pair of rectangular bones separated by a mesial suture,
located in the anterior portion of the skull, between the two
maxillas pairs. Its posterior portion contacts the vomer and
presents a pair of foramina praepalatinum (one in each pair
unit). The premaxilla surface is strongly trabeculated, mostly
along the anterior border (Fig.9).
Fig. 8 Lateroposterior view
from Trachemys dorbigni
skull (CHR-153) with four
foramina in the exoccipital (a)
and another specimen (CHR-
16) with three foramina in the
exoccipital bone (b). Condylus
occipitalis (co); exoccipital
(ex); foramen jugulare posterior
(p); foramen nervi hypoglossi
(fnh); parietal (pa); supraoc-
cipital (so); fourth foramen
in exoccipital (black arrow);
tuberculum basioccipitale (yel-
low arrow)

Zoomorphology
1 3
Prootic
A paired bone located in the floor of the fossa temporalis
superior. The prootic forms a large foramen, the foramen
stapedio-temporale, very near to the conspicuous narrowing
of this bone formed by a brief lateral process of the parietal
bone. Laterally, the prootic contacts the quadrate and poste-
riorly the squamosal.
Supraoccipital
Single bone that forms the posterior portion of the skull
and also the posterior portion of the crista supraoccipi-
talis. Anteriorly, it contacts the parietal bone (contact that
extends from the fossa temporalis superior until the most
dorsal portion of the crista supraoccipitalis) and laterally
the opisthotic. The supraoccipital bone also forms the dorsal
margin of the foramen magnum.
Squamosal
Paired bone located at the posterolateral portion of the skull,
forming the lateral wall and a section of the fossa temporalis
superior floor. It contacts anteriorly with the prootic (only on
the fossa temporalis superior floor) and with the quadrate. In
some specimens, it may extend, on one or both skull sides,
to the foramen stapedio-temporale (Fig.10). Medially, the
squamosal is articulated with the opisthotic and also may
be shortly articulated with supraoccipital (not in all speci-
mens). The contact with supraoccipital and parietal is also
very short and can’t be seen in all specimens.
In the lateral view, it is also articulated with the quadra-
tojugal and, in some specimens, may articulate with the pos-
torbital. Two crests form in the squamosal posterior aspect:
one dorsally, that extends in the medial direction and another
one lateral and inclined in a ventral direction (Fig.11).
Vomer
The vomer is a single elongated bone located in the medial
portion of the skull in the ventral view. The bone center
has a narrowing outline followed by an abrupt anterior wid-
ening. The vomer forms the margin and the walls of the
apertura narium interna. Laterally it contacts the maxilla
and palatine, posteriorly the pterygoid and anteriorly con-
tacts the premaxilla. There are a pair of foramina at the
suture between the vomer and the premaxilla that may be
absent in some specimens (in a symmetrical or asymmetrical
conformation), and also may present variations in their posi-
tion, such as posterior displacement of one of the foramens,
generating an asymmetric arrangement (Fig.10a, b).
Fig. 9 Palatal view of anterior portion of Trachemys dorbigni skull.
a Absence (CHR-142) and b presence of asymmetrical design (CHR-
151) of foramen praepalatinum (arrows); maxilla (mx); palatine (pl);
premaxilla (pm); vomer (vo)
Fig. 10 Detail of the fossa temporalis superior floor of Trachemys
dorbigni skull (CHR-144). Squamosal contacting the border of the
foramen stapedio-temporale (arrow); prootic (pr); quadratojugal (qj);
quadrate (qu); opisthotic (op); parietal (pa); postorbital (po); squa-
mosal (sq); supraoccipital (so)

Zoomorphology
1 3
Palatine
Paired bone of the skull in the ventral view, located later-
ally to the vomer and posteriorly to the maxilla. Laterally, it
contacts the maxilla and quadratojugal, and posteriorly con-
tacts the pair of pterygoids. The palatine forms the margin
of several openings in the palatal view, such as the foramen
orbito-nasale and the foramen palatinum posterius.
Mandible osteology
The dental, coronoid, surangular, and articular bones can be
seen in the lateral view of the lower jaw of T. dorbigni. A
large concave depression extends from the center to the pos-
terior portion of the lower jaw, formed by the insertion of the
mandibular adductor muscle (Fig.12b). Medially, the lower
jaw is composed by the dental, coronoid, angular, prearticu-
lar, articular, and sulcus cartilaginis meckelli (Fig.12a).
Angular
This bone forms part of the ventral portion of the mandible
and is visible only in the medial view. It has a trapezium
shape, is located between the dentary and the prearticular
bones and contacts ventrally with the sulcus cartilaginis
meckelli. Due to its conspicuous shape, there is an antero-
dorsal-narrowed process that enters the sulcus cartilaginis
meckelli and articulates with dentary bone. A second pos-
teroventral process has a continuous and descending suture
that contributes slightly to the ventral margin of the foramen
intermandibularis caudalis.
Articular
Posterior bone in the lower jaw, responsible for the articula-
tion of the mandible with the skull, via the quadrate man-
dibular condyle. Its posterior portion is broad and flat, and
this region is called the mandibular articular area, where
the foramen posterius chorda tympani is also located. The
articular contacts laterally with the prearticular and medially
with the surangular.
Coronoid
The most dorsal element of the lower jaw. The coronoid has
a notable, rounded dorsal process that fits the cheek emar-
gination. The coronoid contacts dorsally with the dentary
and anteriorly with the surangular. Its medial face forms a
triturating surface part and it is totally covered by the horny
beak. Below the horny beak is the foramen intermandib-
ularis medius located exactly at the articulation with the
prearticular. This bone also has a dorsal process called the
coronoid process.
Fig. 11 Occipital view of the Trachemys dorbigni skull (CHR-111).
Squamosal crests (arrows); aperture glossopharyngeal (ag); basioc-
cipital (bo); foramen jugulare posterius (p); foramen nervi hypo-
glossi (fnh); opisthotic (op); pterygoid (pt); quadrate (qu); squamosal
(sq)
Fig. 12 Medial view of the right mandibular branch (a) and lateral
view of the left branch (b) of Trachemys dorbigni. Angular (ang);
articular (art); coronoid (cor); dentary (den); prearticular (pra); suran-
gular (sur). Author’s drawing

Zoomorphology
1 3
Dentary
The largest mandibular bone, where adhesion of a large part
of the horny beak occurs. The anterior portion of the dentary
is pointed in shape. In the lateral view, the dentary bone con-
tacts the coronoid and the surangular (lateral) and forms the
foramen dentofaciale majus in the central portion of the bone.
From the medial view, the dentary has the cartilaginis
meckelli sulcus, which extends horizontally to the intermand-
ibularis foramen medium (large anterior opening of the Meck-
el’s fossa). The dentary articulations by this view occur within
the sulcus cartilaginis meckelli, with the angular, prearticular
and coronoid bones. The articulation with the prearticular
occurs only within the sulcus cartilaginis meckelli. The fora-
men alveolar inferior is present in the posterior portion of the
sulcus cartilaginis meckelli, and in most cases is covered by
the prearticular and, therefore, is not visible in the medial view.
The occlusal surface also occurs within the dentary, limited
by two crests: the labial (more laterally) and the tomial (more
medially) ridges.
Prearticular
Posterior bone of the mandible in the medial view. The
prearticular contacts posterodorsally with the coronoid, poster-
oventrally with the angular and posteriorly with the articular.
Its posterodorsal portion forms the surangular medial ridge and
the medial wall of the Meckel’s fossa. The bone is irregularly
shaped and has several important foramina on its body. Among
these are the foramen intermandibularis caudalis and the fora-
men intermandibularis oralis, both located in the prearticular-
angular sutures, and also the foramen anterius chorda tympani
in the contact with the coronoid.
Surangular
An irregularly shaped bone of the mandible in the lateral
view. Located posterodorsally to the dentary and posterior
to the coronoid. It forms a dorsal process located posteri-
orly to the mandibular articular area, and laterally to this, an
innominate foramen (until the publication of this study). In
T. dorbigni, the surangular contributes to the configuration
of the coronoid process. On the lateral side, the surangular
has a remarkable foramen called the foramen nervi auricu-
lotemporal is which, in some specimens, may be formed by
more than one aperture.
Discussion
There are several characteristics highlighted in this
description of the syncranial osteology of T. dorbigni that
are shared with other species of Emydidae. The cranial
shape and design, and the arrangement, shape and bone
boundaries are conserved, not only among the Emydidae,
but also among the Cryptodira as a whole. The variations
in the cranial anatomy reported in the present study have
also been found in other species of chelonians, and are
generally related to intraspecific variations, interspecific
variations, or sexual dimorphism (Bertl and Killebew
1983; Bever 2009; Gaffney 1979; Jones etal. 2012).
Some characteristics previously described by Souza
etal. 2000 for T. dorbigni, were shown to be different
and/or variants in the present study. The frontal bone was
previously described in T. dorbigni, as one of the orbital
bone components. However, our results demonstrate that
this characteristic is not present in all individuals of the
species and there are considerable variations in this pat-
tern, such as the symmetry (or asymmetry) of the isolation
of the frontal bone from the fossa orbitalis margin.
The different morphologies of frontal bone were already
reported in other species (Jones etal. 2012). Jones etal.
(2012), observed variations in frontal arrangement related
to the size of individuals. In Caretta caretta, small speci-
mens showed the junction between the frontal, prefrontal
and postorbital rather close to the orbital margin, whereas
in larger specimens, this junction occurs more medially,
culminating in a total exclusion of the frontal from the
orbit. In Lepidochelys kempii Garman, 1880, Lepidochelys
olivacea (Eschscholtz, 1929), Chelonia mydas (Linnaeus,
1758), and Eretmochelys imbricata (Linnaeus, 1766), the
frontal is present in a large part of the orbital margin and
variations in this pattern are not mentioned. However, in
the Jones etal. (2012) article, a specimen of Lepidochelys
sp. presented a distinct characteristic, and this variation
was enough for the authors to call into question the correct
taxonomic determination for this specimen. Was found an
asymmetric intraspecific variation in the frontal in only
one sample of 80 specimens of Pseudemys texana (Bever
2009).
Two genera of fossil cryptodiras, Neurankylus and Hay-
emys, formerly considered synonyms, were decisively con-
sidered two distinct taxa due in part to the absence of contact
between the frontal and the margin of the dorsal orbit in
Neurankylus (Brinkman and Nicholls 1993).
The frontal contribution to orbit rim was considered a
primitive character for Testudinata by Joyce 2007; however,
this character shows several reversals within Cryptodyra.
Joyce and Bell (2004) reinforce the importance of includ-
ing a larger sample of extant testudinoids specimens for a
reliable assessment of character intraspecific variation, as
presented by Yasukawa etal. (2019). Yasukawa etal. (2019)
determined three possibles morphologies for Geomydines
turtles: usually present, without prefrontal–postorbital con-
nection; sometimes absent, with weak prefrontal–postorbital
connection; and absent with strong prefrontal–postorbital

Zoomorphology
1 3
connection. T. dorbigini seems to be included in the pro-
posed second character state.
The prefrontal smooth surface seen in T. dorbigni is
a dominant character among turtles (Joyce 2007). Pro-
ganochelys quenstedti is the only Testudinata known with
prominences and ridges in the dorsal prefrontal plate, which
resemble the brown ridges of basal humans (Joyce 2007).
The absence of nasal bone in T. dorbigni portrays a
derived character among Testudines and partially com-
mon in extant species. The presence of the nasal in current
Testudines is restricted to Chelidae and has different mor-
phologies in different species, being absent only in Che-
lus (Gaffney 1977). The nasal bone presence, on the other
hand, seems to occur in the vast majority of extinct groups
(Gaffney etal. 2007). Gaffney etal. (2007) sets Chelonioidea
(sea turtles group) as containing nasal bone based on fos-
sils species. However, it is known that currently living sea
turtles (for example Eretmochelys, Chelonia, Caretta, Lepi-
dochelys, and Dermochelys) do not have this bone, despite
being inserted within Chelonioidea (Hiramaya 1994). The
phylogeny of Chelonioidea based on morphological charac-
ters proposed by Hiramaya (1994) presents the absence of
the nasal as a derived character and details the occurrence
of the bone in different species of the group.
The absence of the supratemporal bone is also a derived
character, since it is restricted to basal taxa (Joyce 2007).
According to the materials of Souza etal. (2000), the
jugal bone of T. dorbigni is part of the caudal margin of the
orbits; however, in the present study, it was verified that this
characteristic is not standardized in the species, and there
are cases in which the jugal has a different configuration.
Gaffney (1979) cited that the jugal is, in most species of
chelonians, a caudal component of the orbital margin, but in
Platysternon and Eubaena species, the jugal is limited ante-
riorly by the postorbital and the maxilla, preventing it from
forming part of the orbital margin, which was also observed
in the present study in some specimens of T. dorbigni. Bever
(2009) described that in P. texana, the jugal bone contains a
prominent lateral plate that forms the posterior margin of the
orbits and the author does not cite any variation in this pat-
tern in the species. Bertl and Killebrew (1983) have pointed
out this variation in the jugal as an important characteristic
to distinguish the species Graptemys caglei HAYNES &
MCKOWN, 1974 (in which the jugal does not form the out-
line of the orbits) and Graptemys versa STEJNEGER, 1925
(in which the jugal forms a considerable posterior margin
of the aperture).
According to Gaffney (1979), the morphology of the
quadrate bone can present different dispositions within the
chelonians group. In Malaclemys, Chrysemys, Kinostern-
ids, and Platysternon, the quadratojugal articulates with
the maxilla, and in the species belonging to the Podocne-
mys, Peltocephalus and Erymnochelys, the quadratojugal
articulates with the parietal. In Graptemys, the quadratojugal
forms the contour of the fossa temporalis superior (as illus-
trated by Killebrew 1979), while in P. texana, there seems
to be no contact, and there is alternating contact with the
maxilla in most specimens (Bever 2009).
The contact between squamosal and parietal is usually
present in turtles that the upper temporal emargination is
absent or poorly developed (Joyce 2007). Although this
contact is present in T. dorbigni, it seems not to be homolo-
gous to the character described by Joyce (2007), once the
articulation occurs in the fossa temporalis superios floor
and the specie has a well-developed upper temporal emar-
gination. The same inference is made for the contact squa-
mosal–supraoccipital in T. dorbigni.
Unlike that found in representatives of Trionychia and
Kinosternoidea, T. dorbigni does not present any ascending
process of the palatines (Joyce 2007). As a result, the ante-
rior extension of the lateral braincase wall is formed only by
the parietal bones.
The relation between the prepalatine foramen and the
nasal anterior artery was described by Gaffney (1972). This
artery originates from the palate and anastomoses with the
nasal tissue. The foramen may be formed by both the vomer
and the premaxilla together (Seidel and Smith 1986) or may
be entirely located in one of the bones (Gaffney 1979). In
P. texana, the foramen praepalatinum can be found either
completely inserted in the premaxilla or exactly in the suture
between the vomer and the premaxilla, and in some cases,
may even be "hidden" by the palatal view due to the vari-
able degree of ossification in and around these foramina
(Bever 2009). In some cases, the foramen praepalatinum
may also be absent, and in these configurations, there is a
caudal opening to the premaxilla called the intermaxillary
foramen (Gaffney 1979). In the skulls of T. dorbigni that
do not have the foramen praepalatinum, the opening of the
intermaxillary foramen was also not found, making further
studies related to the anatomy of the head involving dis-
sections necessary to diagnose the position of the anterior
nasal artery.
According to the illustrations of Gaffney (1977), the
vomer in Hydromedusa tectifera COPE, 1869, Chelodina
expansa CINZA, 1957 and Chelus fimbriatus is small when
compared to the palatines. In the papers of Gaffney (1972,
1979), Bertl and Killebew (1983), Souza etal. (2000) and
Jones etal. (2012), illustrations always demonstrate the
vomer with its caudal limit at the caudal palatal limits, and in
some cases, the vomer appears to be slightly more developed
as observed in Phrynops gibba. However, in these cases, it
is not possible to affirm if this characteristic is considered
polymorphic or not for these species, since it is a discrete
variation.
The presence of a fourth foramen in the exoccipital bone
in the posterior view of the skull, may be explained by the

Zoomorphology
1 3
structure of the hypoglossal nerve (which crosses the fora-
men of the hypoglossal nerve), which is a complex of fibers
that can cross the skull for two or three foramen (Gaffney
1979). As such, the fourth hole found in some T. dorbigni
skulls may be a third foramen of the hypoglossal nerve.
Gaffney (1979) also says that in some situations which only
two foramina are visible, there was a fusion between the
two most anterior foramina. That’s why it is only possible
to visualize only two foramina from the external view of the
skull, instead of three. Observations about this foramen were
not found in other studies related to the cranial morphology
of chelonians.
Perhaps the occurrence of a surangular innominate fora-
men is not only seen in T. dorbigni. Gaffney (1979) affirms
that in some Cryptodiras presents a foramen in the suran-
gular bone that communicates with auriculotemporal nerve
foramen and the Meckel’s fossa. Although the description
of this unknown foramen coincides with that found in the
present study, Gaffney (1979) does not describe its exact
location in the bone and does not present any illustration of
the foramen. Therefore, it is imprudent to state that it is the
same structure reported in T. dorbigni.
Bertl and Killebrew (1983) described a series of sexually
dimorphic cranial features that differentiate two species of
Graptemys (Emydidae). Similar morphological variations
were also found in T. dorbigni, but these were not shown
to be related to sexual dimorphism, since the different mor-
phologies occur in both males and females.
In P. texana, dimorphic characters related to cranial mor-
phology were also reported (Bever 2009). The author sug-
gests that, in males, the dorsal margin is flattened in the
regions between the orbits and at the height of the occipital
crest. Such variation can also be observed in T. dorbigni;
however, we considered the oscillation to be very small, and
it did not differ systematically between males and females,
and thus was not mentioned in the results of this study.
The mandibular morphology, when compared to other
species, seems very conserved within chelonians and few
variations are observed (Bertl and Killebrew 1983; Bever
2009; Jones etal. 2012; Gaffney 1979). One of the main
differences is in the visibility or presence/absence of man-
dibular foramina between species. However, it also appears
that the details of this structure are often neglected in oste-
ological studies, since all the foramina described for the
chelonians by Gaffney (1972) were found in T. dorbigni.
The occurrence of an innominate foramen in the surangu-
lar found in this study, has apparently already been found
in other cryptodiras, such as Staurotypus, Terrapene and P.
texana (Bever 2009; Gaffney 1979).
The variations found in the morphological pattern of the
T. dorbigni skull in this study, as well all the details not
described by Souza etal. (2000), is unprecedented for the
specie. These results differ from those found by Souza etal.
(2000) in T. dorbigni, probably because of the large sample
size (83 skulls) analyzed in this article. Souza etal. (2000)
described the osteology of the species, using 16 specimens
(among them, males, females and juveniles), and their
descriptions and illustrations were based only on four (three
females and one male), which was possibly insufficient to
show the great variability and anatomical richness that these
structures (skull and mandible) can present in this species.
The great variability in the morphology of the T. dorbigni
skull reveals that although it shows similarities to the other
species of Emydidae, it has considerable plasticity in the
morphology of the skull, whereas the mandible tends to be a
conserved structure and to maintain an intra and interspecific
pattern among the chelonians.
Based on the results obtained through the osteological
description, it is possible to conclude that T. dorbigni skull
presents considerable variations in the shape and pattern
of bone articulation between the dermocranial elements.
Although it has general characteristics like others Emydidae
species. Therefore, it is possible to state that there is con-
siderable intraspecific variation in the Trachemys dorbigni’s
skull.
Acknowledgements We thank Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES) for the scholaship funds provided.
Funding Masters scholarship granted by Coordenação de Aper-
feiçoamento de Pessoal de Nível Superior (CAPES) for Priscila Rock-
enbach Portela and Róger Jean Oliveira.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval This article does not contain any studies with human
participants or animals performed by any of the authors.
Informed consent Additional informed consent was obtained from all
individual participants for whom identifying information is included
in this article.
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