Table Of Content© Zoological Institute, St. Petersburg, 2008
Descriptive osteology of Gymnocorymbus ternetzi
(Teleostei: Characiformes: Characidae)
N.G. Bogutskaya, A.M. Naseka & I.V. Golovanova
Bogutskaya, N.G., Naseka, A.M. & Golovanova, I.V. 2008. Descriptive osteology of
Gymnocorymbus ternetzi (Teleostei: Characiformes: Characidae). Zoosystematica Rossica,
17(2): 111-128.
The purpose of this paper is giving an extensive overview of the cranial skeleton of Gym-
nocorymbus ternetzi (Boulenger, 1895) in a form of a formalized scheme that reflect its
Bauplan (German for building plan, blueprint; plural: baupläne or bauplaene), a term in
biology referring to the common new and original [homologous] properties of the members
of a systematic group [taxon]). Each element of the Bauplan can be described by a set of
parameters, i.e., size, shape, structure, material composition and position. Though Bauplan
is undoubtedly an abstraction, it is a necessary abstraction to be used in phylogenetic analy-
sis with preference to “ingroup” and “outgroup” comparisons.The cranial osteology of
black tetra Gymnocorymbus ternetzi (Boulenger, 1895) is described based on the study of
larvae, juvenile and adult specimens. Provided are Latin terms and some English equiva-
lents as well remarks on origin, homology and terminology for each cranial bone discussed.
N.G. Bogutskaya, Zoological Institute, Russian Academy of Sciences, Universitetskaya
nab. 1, St. Petersburg 199034, Russia. E-mail: [email protected]
A.M. Naseka, Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1,
St. Petersburg 199034, Russia. E-mail: [email protected]
I.V. Golovanova, St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg
199034, Russia.
Introduction group. A close relationship between the group, until
then referred to as the Ostariophysi, and the
Fishes are known to have a morphologically Gonorhynchiformes, was demonstrated by Rosen &
complex and highly kinetic skull (Ferry-Graham & Greenwood (1970), based on evidence of the caudal
Lauder, 2001). The cranial musculo-skeletal system skeleton, the presence of a fright reaction mecha-
of adult teleost fishes consists of about 60 intercon- nism, swimbladder morphology, presence of nuptial
nected skeletal parts that are moved by an approxi- tubercles and a striking similarity in the mouth
mately equal number of muscles (Aerts, 1991). opening mechanism in Phractolaemus ansorgii
Morphological studies on the skeletal morphology (Gonorhynchiformes, Phractolaemidae) and Bivi-
of Ostariophysi have already been done by many branchia (Characiformes, Hemiodontidae). The
authors, although the nomenclature of the skeletal, fact, however, that in Gonorhynchiformes no “real
especially cranial, structures in these papers demon- sign of vertebral differentiation that would suggest a
strated a high degree of inconsistencies, which re- condition paralleling the development of Weberian
quired an initial priority of this study: to provide a ossicles”, could be observed that convinced them of
conclusive nomenclature, which allowed compari- similar functionality, in a broad sense, as the Webe-
son with other taxa. Besides, the ontogeny of the rian apparatus, resulted in the subdivision of the
skull could provide substantial information concern- Ostariophysi in the Anotophysi (Gonorhynchifor-
ing the origin of bones, whereas the study of the mes) and the Otophysi (Ostariophysi s.s.) (Rosen &
cranial lateral-line system could give data on the Greenwood, 1970). A first detailed survey of the
true nature of canal bones. ostariophysan interrelationships was given by Rob-
erts (1973). He stated that “evidence from caudal
Regan (1911a, 1911b) considered the Ostario-
skeleton morphology supports relationships be-
physi to be a group of species which share the
tween Clupeomorpha and Ostariophysi, and be-
common feature of the Weberian apparatus. The
tween Clupeomorpha and Gonorhynchiformes, as
Ostariophysi, according to Regan (1911a, 1911b)
well as between Gonorhynchiformes and Ostario-
comprised the suborders Cyprinoidea and the
physi.” He opposed against the notion that characins
Siluroidea. The Characiformes, belonging to the
and cyprinids would be more closely related to each
Cyprinoidea, were regarded as the least specialised
112 N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi • ZOOSYST. ROSSICA Vol. 17
other than to the catfishes, consequently raising the al., 1992; Cubbage & Mabee, 1996; Bird & Mabee,
latter to the same level as the former two. His order 2003), characids (e.g. Bertmar, 1959; Vandewalle et
of Cypriniformes than corresponds with the Oto- al., 2005; Miquelarena et al., 2005) and catfish (e.g.
physi of Rosen & Greenwood (1970), containing Bamford, 1948; Geerinckx et al., 2005, 2008) (see
the three suborders: (1) Characoidei, (2) Cyprinoidei also references cited in these publications).
and (3) Siluroidei. A more extensive comparison of The purpose of this paper is giving an extensive
ostariophysan groups by Fink & Fink (1991, 1996) overview of the skeleton of Gymnocorymbus ter-
lead to a new classification of ostariophysans. Fink netzi (Boulenger, 1895) in a form of a formalized
& Fink (1996) gave strong morphological evidence scheme that reflect its Bauplan (German for
for the phylogenetic relationships of the Otophysi building plan, blueprint; plural: baupläne or
(comprising herein four orders, the Cypriniformes, bauplaene), a term in biology referring to the
Characiformes, Siluriformes, and Gymnotiformes). common new and original [homologous] properties
Their results show, of the major clades, the fossil of the members of a systematic group [taxon]). Each
Chanoides to be sister to all remaining members of element of the Bauplan can be described by a set of
otophysans (placed in the Cypriniphysi), with the parameters, i.e., size, shape, structure, material
Cypriniformes being the primitive sister taxa to the composition and position (Verraes, 1981; Adriaens,
remaining three groups (the Characiphysi), and 1998). Though Bauplan is undoubtedly an abstrac-
Characiformes being sister to the clade (the tion, it is a necessary abstraction to be used in phy-
Siluriphysi) of Siluriformes and its sister group the logenetic analysis with preference to “ingroup” and
Gymnotiformes. “outgroup” comparisons.
Several hypotheses have been proposed concern- The nomenclature used for the developing skele-
ing the evolutionary distribution pattern of ostario- tal structures is based principally on the works of de
physan fishes.As for today, not all groups of Beer (1937), Harrington (1955), Daget (1964), Pat-
ostariophysans show an identical distribution. The terson (1977) and Geerinckx et al. (2005). A discus-
Siluriformesshow a cosmopolitan distribution, sion on homologies and terminology of the bones is
whereas the Gymnotiformes are confined to South given below in respective places.
America.The majority of the ostariophysans can be
categorised as primary freshwater fishes. Secondary Material and Methods
fresh water fishescan be found in Cypriniformes
(Cyprinidae), Characiformes and Siluriformes (e.g.,
The ontogeny of the bones was observed in the
Clariidae, Siluridae,Claroteidae, Pangasiidae, Lori-
developmental stages of Gymnocorymbus ternetzi.
cariidae), whereas peripheral species have been
Specimens, obtained from an aquarium shop, were
observed in Gonorhynchiformes(Chanidae,
fixed in a 4% buffered formaldehyde solution, and
Gonorhynchidae) and Siluriformes (Aspredinidae,
used for in toto clearing and staining at different
Ariidae and Plotosidae) only (Roberts, 1975;
time intervals according to Hanken & Wassersug
Teugels, 1996; Nelson, 2006).
(1981), with trypsine replaced by a 3% KOH solu-
The Otophysi included (as calculated in 2005, tion. The examined material ranges from 4.0 mm
Nelson, 2006) 64 families, 1,068 genera, and 7,894 norochord length (NL) larvae (9 days after hatch-
species. It is now included four orders, Cyprinifor- ing) to 65.0 mm standard length (SL) adults (three
mes (eight families: Cyprinidae, Psilorhynchidae, months after hatching).
Gyrinocheilidae, Catostomidae, Balitoridae, Cobiti-
dae, Nemacheilidae and Botiidae; two latter families
Categories of skeletal structures in terms of
had earlier been treated as subfamilies of Cobitidae,
bone histology and embryonic development
later of Balitoridae, and now as distinct family, e.g.
Nalbant & Bianco, 1998; Tang et al., 2006; Šlech-
Several different types of cartilage could be dis-
tová et al., 2008), Characiformes (18 families),
tinguished in Teleostei: (1) cell rich hyaline carti-
Siluriformes (about 15 families). About 64% of all
lage, (2) matrix rich hyaline cartilage, (3) fibro/cell-
freshwater fishes can be grouped within the
rich cartilage, (4) elastic/cell rich cartilage, (5)
Ostariophysi, where they can be found world wide,
‘Zellknorpel’ (could be observed in the oral barbells
with exception of Antarctica, Greenland and New
and the gill filaments), (6) scleral cartilage (support-
Zealand.
ing the eye ball) (Benjamin, 1989, 1990). The larval
There are many publications, including classical
skeleton of fishes is constituted of cartilaginous
ones, on descriptive and comparative osteology of
structures. In the whole skeleton, there are about 60
fishes of the group Otophysi (e.g. Nawar, 1954;
cartilage precursors that further develop into ossi-
Harrington, 1955; Weitzman, 1962; Vandewalle,
fied structures. The cranial cartilage may be divided
1977; Cabuy et al., 1999; Huysentruyt & Adriaens,
into the chondrocranium cartilage and the pharyn-
2005; Serra & Langeani, 2006). Ontogenetic devel-
geal arch cartilage which respectively develop into
opment of the skeleton has been described in a
chondral bone elements of the neurocranium and
number of papers on cyprinids (e.g. Vandewalle et
ZOOSYST. ROSSICA Vol. 17 • N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi 113
the splanchnocranium. The pharyngeal arch carti- gariepinus, for example, it was found only in the
lage includes cartilages of seven pharyngeal (or hyoid bar (Adriaens, 1998). Apart from peri-
visceral) arches which are also called the mandubu- chondral bones (and endochondral bones), the so-
lar arch, the hyoid arch, and five branchial (or gill) called parachondral bones can be observed in
arches. Each arch possesses its own cartilage com- some skeletal regions. Parachondral ossification,
ponents. The chondrocranium cartilage consists of although lying closely against cartilage or peri-
neurocranial trabecula, parachordal cartilage, eth- chondral bone, is still separated from it by at least a
moid cartilage, otic capsule and other components. layer of perichondrium and periosteum, or two lay-
Most cartilage precursors of the bones described in ers of periosteum, respectively.
the paper are mentioned in respective places below. INTRAMEMBRANOUS BONE develops directly
Distinguished are three main categories of bones: from a mesenchymal condensation and lacks any
(1) cartilage bone, (2) dermal bone, and (3) mem- cartilaginous precursors, neither ontogenetically nor
brane bone (e.g. Patterson, 1977) though the two phylogenetically (Patterson, 1977). Intramembra-
latter types are often considered as one type called nous bones that are formed superficially (in connec-
intermembranous bone, or dermal bone, with two- tion with the ectoderm) are commonly referred to as
three subtypes. A fourth type, which could not be dermal bones and those lying deep in the mesoderm
grouped in one of them, involves the so called as membrane bones.
chondroid bone (Huysseune, 1986; Huysseune & Dermal bones may enclose a canal of the cranial
Verraes, 1990). Of all four types of bone, separate lateral-line system or may not. A canal bearing bone
representatives have been observed in G. ternetzi. consists of the membranodermal component and the
Additionally, fusions occurred between the different neurodermal component that fuse together in ontog-
types of bone: 1 - perichondral bone and membra- eny. Early dermal bones all are simple and plate-
nous bone, 2 - perichondral bone and dermal bone, like. Growth and bone deposition appears to occur
3 - perichondral bone and chondroid bone, 4 - der- especially at the margins of these plates, reflected by
mal bone and dermal bone. These categories of the concentration of osteoblasts. Later on, dermal
bones are reviewed by Adriaens (1998). bones start to form apolamellae as well, perpendicu-
CARTILAGE BONE (or cartilage replacement lar to its surface.
bone). Bones developed from a cartilage precursor. Membrane bones are those bones that ossify “in
During ontogeny perichondral osteoprogenitor cells membrane deep in the mesoderm, with no ontoge-
differentiate into osteoblasts (Meunier & Huysse- netic or phylogenetic connection with the ectoderm”
une, 1992). As they surround the cartilaginous struc- (Patterson, 1977). These bones involve those that
ture, they initiate perichondral ossification, which are homologous with cartilage bones in more primi-
is the primal phase of ossification. By producing a tive vertebrates, as well as sesamoid bones and out-
thin layer of osteoid, the osteoblast may or may not growths of cartilage bones. Only three bones are
become enclosed in this matrix, which may subse- referred to as membrane bones in Danio (Brachy-
quently become mineralised by hydroxy-apatite danio) rerio, intercalary (in the oric region), and
crystals. Whether osteoblasts become enclosed, claustrum and tripus (in the Weberian apparatus)
consequently differentiating into osteocytes, or re- (http://zfin.org/action/anatomy).
main at the surface of the continuously added bone CHONDROID BONE. At many articulations, an
matrix, results in the presence of cellular or acellular unusual kind of tissue, closely resembling cartilage
bone. Lower teleost fishes, including ostariophysans invaded by bone, can be observed. These articula-
(zebrafish), are reported to lack acellular bone (Par- tions involve those between (1) the maxillary bone
enti, 1986), whereas acellular bone is most fre- and the autopalatine bone, (2) the autopalatine bone
quently observed in higher taxa (again with some and the lateral ethmoid bone, (3) the autopalatine
exceptions) (Meunier & Huysseune, 1992). At a bone and the antorbital bone, (4) the lower jaw and
later stage, cartilage has been observed to become the suspensorium, (5) two dental bones (Adriaens,
mineralised as well, at the close connection with the 1998; Gill et al., 2006).
perichondral bone. Resorption of this cartilage is
generally preceded by perichondral ossification. Description and discussion
Such chondroclastic resorptions may be accompa-
nied by the invasion of a blood vessel into the carti-
As Romer (1947) has pointed out, the determina-
lage, consequently supplying new osteoblasts. The
tion of precise homologies between the skull bones
thus formed intracartilaginous canal may become
of different groups of fishes presents great difficul-
lined with bone. Even more, the cavity formed
ties. The homology of many teleost skull bones is in
within the perichondral bone, as a result of exten-
question. The latest trend in Anglicising of scientific
sive cartilage resorption, may be filled with bony
language is a major contributor to term prolifera-
trabeculae. Such an intracranial ossification is then
tions (e.g., dental, dentary or lacrymal, lachrymal,
referred to as endochondral ossification. The latter
lacrimal). In an ontogenetic context, this gives even
category of ossifications is quite rare; in Clarias
114 N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi • ZOOSYST. ROSSICA Vol. 17
more problems, e.g., dentary is sometimes used Os ethmoideum laterale [os ethmoidale laterale;
when referring to both the (1) os dentale, (2) the lateroethmoideum]. The lateral ethmoid is a large,
fused complex between the os mentomeckelian and paired bone of the mixed origin. The lateral ethmoid
the os dentale, or (3) the fused complex between the wing, or lateral process, is composed largely of
latter two and the os spleniale (Adriaens, 1998). We intramembranous prefrontal derivation (Weitzman,
provide Latin terms and some English equivalents 1962) while the medial portion is apparently of
as well remarks on origin, homology and terminol- endochondral origin from the cartilages separating
ogy for each cranial bone discussed below. the olfactory region from the orbit (the laminae
In general, the skeleton can be defined and subdi- orbitonasales). It was shown for cyprinids that it
vided as all the cartilaginous and bony elements arises from both perichondral and endochondral
comprising the exoskeleton (or dermoskeleton) ossifications (Harrington, 1955). Compaing the
which includes the dermocranium, secondary pecto- developmental stages of G. ternetzi we found two
ral girdle and scales, and the endoskeleton. The origins of ossifications which spacially correspond
latter has a somatic axial component comprising the to the chondral and dermal prefrontal ossifications.
neurocranium, vertebral column and paraxial ele- Bordered by the ethmoid anteriorly and overlain
ments, a somatic appendicular component compris- by the frontal dorsolaterally, the lateral ethmoid
ing the median fins, paired fins, radials, pterygio- forms the upper anterior wall of the orbit. Each
phores and fin rays, and a visceral component, the lateral ethmoid projects downward from under the
splanchnocranium (or viscerocranium), comprising anterior region of each frontal, and lies lateral to the
the mandibular arch, the hyoid arch and the bran- anterior part of the rhinosphenoid. Although the
chial arches (Coad, 2008). lateral ethmoids approach each other medially, they
do not reach the midline and do not contact each
Cranium: neurocranium other but do contact the anterior edge of the rhino-
Ethmoid region [=olfactory region] (Figs 1, 2). sphenoid and the ethmoid. On its anterior surface
and between its median and lateral regions, the lat-
Os ethmoideum [os mesethmoideum]. The eth-
eral ethmoid bears a very narrow spur that extends
moid [mesethmoid or median ethmoid] is a median
anteriorly and medially to contact the dorso-
unpaired bone of the mixed origin being composed
posterior surface of the rectangular portion of the
of both supraethmoidal (dermethmoidal) compo-
vomer. The lateral portions of the lateral ethmoids
nent and a contribution from the ethmoid cartilage
extend downward as a wide triangular process (Figs
that ossifies as a perichondral lamellae ensheathing
1, 2, leth) to the upper lateral edge of the ectoptery-
the nasal septum anterodorsally and laterally. In
goids. The posterior surface of the ethmoid above
cyprinids, the dermal and chondral ossification are
the rhinosphenoid has a median fossa, the anterior
commonly treated as separate elements, os supra-
myodome, for the origin of the superior oblique eye
ethmoideum (supraethmoid) and os meseth-
muscles. The lateral ethmoid forms one half (the
moideum (mesethmoid).
lower one) of the outer margin of the olfactory fo-
The ethmoid projects forward from under the an-
ramen which is rather large. The posterior section of
terior edge of the frontals, meets the lateral ethmoids
the lateral ethmoid contribution to the olfactory
posterolaterally, and the vomer and parasphenoid
foramen is formed by the bone itself while the ante-
ventrally in synostoses. Anteriorly the ethmoid bone
rior section by the spur contacting the lateral margin
ends in a pointed process which forms the anterior-
of the vomer. Ligamentous tissue suspends the up-
most portion of the neurocranium (Fig. 1, eth). This
per anterior tip of the maxillary bone to the lateral
part of the anterodorsal region of the ethmoid is
ethmoid wing.
called the “ethmoidal spine” by Weitzman (1962);
laterally from the ethmoidal spine the flattened
plates serve as joint surfaces for the reception of the Os vomer [os vomerale]. The vomer is a fre-
ascending processeses of the premaxillaries. In the quently median unpaired or paired dermal bone in
dorsal aspect, the ethmoid is narrow, about two the middle of the roof of the mouth covering the
times longer than wide. Its posterior part is about as ethmoid ventrally and in front of the parasphenoid.
wide as the anterior part, and the posteriormost ex- There is still a big debate about the using of the
tremety is markedly concave forming two horns name vomer for it was shown long ago that the
(latero-dermethmoids of some authors) extending vomer in mammals is homologous with with the
posteriorly to contact the frontals. Thus, the parassphenoid rather than with this bone in fishes.
posterior ethmoid margin forms a part of the ante- Many authors use the name os praevomer [os
rior margin of the anterior (prepineal) fontanel (the praevomerale] (prevomer). Compaing the develop-
anterior part of the large dorsomedial cranial fon- mental stages we found no paired precursors of the
tanel) (Fig. 1, ppf). No or few foramina pierce the vomer.
surface of the ethmoid. The vomer is toothless; it is somewhat convex
dorsally and concave ventrally. The upper anterior
portion of the vomer is in contact with the parts of
ZOOSYST. ROSSICA Vol. 17 • N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi 115
the lateral ethmoid wings by a synchondral joint ossified only in the adults (Fig. 1, eb). In the smaller
surface. The vomer is located almost vertically be- specimens the frontal bones are relatively farther
cause of the big difference between the depths of the apart than in the older specimens. Ventrally the
ethmoid and sphenotic regions of the neurocranium. frontal bears the orbital lamella, which lies external
The dorsal surface of the anterior region of the to and is applied to the dorsolateral surface of the
prevomer contacts the ventral surface of the eth- pterosphenoid, the orbitosphenoid, and the anterior
moid. The posterior, triangular portion is thin. This region of the sphenotic. The supraorbital sensory
portion, the shaft of the vomer, inserts in a well canal after leaving the nasal enters the frontal at its
defined concavity on the anteroventral surface of the anterior edge. The canal then passes backward hav-
parasphenoid. The anterior, widened, portion of the ing two main branches, the mesial, or epiphyseal
prevomer is thickened, has a slightly concave ante- branch, and the posterior one. The epiphyseal
rior margin, and dorsally forms a synchondral joint branch (Fig. 1, ebc) extends medially over the
surface for the ethmoid. Two anterolateral projec- epiphyseal bar and opens by a terminal pore with no
tions of the vomer extend toward the upper tips of communication to its counterpart. The posterior
the maxillaries and lie below lateral wings of the branch continues backward in the frontal to enter
ethmoid bone. Centrally and in the sagittal plane the the parietal bone at the middle of its anterior edge.
vomer bears a dorsal lamella that contacts a similar The frontal bone(s) is a part of the cranial roof
lamella of the ethmoid. The vomerine lamella is composed of the dermal bones covering the neuro-
rather deep and of almost the same size as the eth- cranium, the nasal, the frontal, the supraorbital, the
moidal lamella. These lamellae together form the parietal and the supraoccipital bones.
deep internasal septum. Gymnocorymbus ternetzi has an orbital ring of
seven bones (Fig. 3); the anteriormost one does not
Os nasale. The nasal is a paired dermal bone, po- bear a sensory canal while six others are associated
sitioned lateral to the dorsal surface of the ethmoid. with the infraorbital canal. The supraorbital bone (os
The nasal bone is transversed by the anteriormost supraorbitale) commonly present in most Otophysi
part of the supraorbital sensory canal; in G. ternetzi is a paired dermal bone that commonly forms the
it is tubular being presented by only the neuroder- anterodorsal margin of the orbit is absent in G. ter-
mal component while any membranodermal com- netzi.
ponent is lacking. The nasal is long, its anterior end
lies laterally to the upper end of the premaxillary Os antorbitale. The antorbital is a paired dermal
ascending process, and the posterior end abuts the bone lying lateral to the nasal bone in front of the
frontal (Fig. 1, n). It encloses two canal segments, eye. This bone lies in the posterior wall of the nasal
and the single pore is located in the middle of the sac and is closely associated posteriorly with the
bone. supraorbital if the latter is present. The antorbital in
A part of the ethmoid region is also the paraspe- characids is not associated with the infraorbital sen-
noid which is discussed below in the sphenoid re- sory canal except presumably secondarily in some
gion. The parasphenoid and the vomer may be also highly modified forms and perhaps cannot be com-
classified as bones of the basicranium, the base of pared directly to the antorbital of Amia. However,
the braincase. its topographic position is the same and Gosline
(1961) apparently concluded that the best name for
Orbital region (Fig. 2). the bone in characids and many other fishes is an-
Os frontale. The frontal bone is a large paired torbital. Homologization of the bone and its termi-
dermal bone that constitutes a great part of the cra- nology in characids and cyprinids in comparison
nial roof. Though as noted in Janvier (1996), what with other lower fishes reviewed by Harrington
are commonly termed the frontals and parietals in (1955), Gosline (1961) and Weitzman (1962). Gos-
actinopterygians, originally taken from human anat- line (1961) supposed that the lachrymal of cyprinids
omy, are homologous with the parietals and postpa- is a compound bone made up of the fused lachrymal
rietals, respectively, of early tetrapods, most authors and antorbital. It is because of the difficulty of ho-
keep using the term frontal in the traditional mean- mologization of elements of the infraorbital series
ing (Nelson, 2006). that Weitzman (1962) designated the infraorbital
Extending from the ethmoid caudad to the parie- elements posterior to the antorbital in characids
tal, posterolaterally each frontal overlaps its respec- simply by number, starting with the first bone bear-
tive pterotic, and just anterior to the pterotic each ing the canal (apparently an equivalent to the lach-
covers its respective sphenotic. The paired frontal rymal).
bones in all specimens examined and at all growth The antorbital bone in G. ternezi is a small trian-
stages are largely separated by a well-developed gular bone considerably narrow and pointed in its
dorsomedian cranial fontanel that is divided by the dorsal part and widened in the ventral part. It does
epiphyseal bar [infrafrontal bar] that is completely not have any contact with the first infraorbital bone
(Fig. 3, anto).
116 N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi • ZOOSYST. ROSSICA Vol. 17
Ossa infraorbitalia [ossa suborbitalia] (Fig. 3). anterior and anterolateral boundary of the orbital
The infraorbital bones [suborbitals bones] are der- foramen and constitutes a part of the sidewalls and
mal bones that are situated under and posterior to floor of the cranial cavity. It is bordered by the
the eye and associated with the infraorbital sensory frontals dorsally, the pterosphenoid posteriorly, and
canal. Name applied to six or more of the circumor- the rhinosphenoid anteriorventrally (Fig. 2, orbsph);
bital bones; in caracids, the following bones are it is positioned medial to the upper part of the eye.
commonly distinguished: infraorbital 1 (lachrymal
or preorbital by some), infraorbital 2 (jugal by ear- Os rhinosphenoideum. The rhinosphenoid is a
lier authors), infraorbital 3 (great suborbital by median cartilage bone which ossified separately
some), infraorbitals 4 and 5, and infraorbital 6 (der- from both the ethmoid and the orbitosphenoid. Ac-
mosphenotic). cording to Weitzman (1962), an a specimen of Bry-
Os infraorbitale 1 [os lacrymale] (Fig. 3, io1). con meeki of 32 mm in standard length, the rhino-
The infraorbital 1 in G. ternetzi is a very shallow sphenoid consisted of two thin discs set side by side,
bone with a poorly ossified both membranodermal sandwiching a disc of cartilage; in larger specimens
and neurodermal components. The canal has two the two lamellar halves of this bone were fused
segments on the bone. The very posterodorsal end along their dorsal edges.
of the bone overlaps only the very anterior extre- The rhinosphenoid projects forward to between
mety of the infraorbital 2. the median edges of the lateral ethmoids and forms
Os infraorbitale 2. The infraorbital 2 is consid- a septum between the olfactory nerves as they issue
erably longer than the infraorbital 1 and deep in its from the orbitosphenoid. All joints of this bone are
posterior part. A very limited posteriordorsal portion synchondral (Fig. 2, rsph).
of the bone overlaps the infraorbital 3. Below both the rhinosphenoid and orbitosphe-
Os infraorbitale 3 (Fig. 3, io3). The infraorbital 3 noid and just above the parasphenoid in the interor-
is the largest element of the infraorbital series. Its bital septum is a small round unpaired ossification
ventral and posterior margins are separated from the (Fig. 2), which appears in specimens of about 35
horizontal and vertical limbs of the preoprcle by a mm SL.
clear distance. The canal has 3 to 5, commonly 4,
segments on the bone. Os parasphenoideum. The parasphenoid is a long
Os infraorbitale 4 and os infraorbitale 5. The unpaired median dermal bone that runs almost the
both infraorbitals 4 and 5 are relatively narrow, with entire length of the neurocranium.
poorly ossified neurodermal component. They do The parasphenoid contacts the vomer anteriorly,
not over lap either each other or the neighbouring and the prootic and basioccipital posteriorly. It is
bones. markedly curved in about the middle of its length
Os infraorbitale 6 (Fig. 3, io6). The infraorbital 6 where it bears a pair of ascending flanges, or as-
is a short bone, its width being about the width of cending wings, which suture with the pterosphe-
the infraorbital 5 or slightly larger. The bone bears noids and prootics of each respective side. The pos-
one canal segment which is a terminal segment of terior myodome lies above the posterior portion of
the infraorbital canal. The canal ends by a pore at the parasphenoid and between ventral extensions of
the upper margin of the infraorbital 6 and does not the prootic. The carotid foramen which occurs be-
communicate with the supraorbital canal. Thus, the tween the anteroventral region of the prootic and the
infraorbital canal in G. ternetzi lacks the most char- parasphenoid just posterior to the scending process
acteristic feature of the dermosphenoticum – an is relatively large, two thirds of its margin is formed
anastomose of the infraorbital canal with the lateral by the notch at the parasphenoid. The ventral keel,
part of the supraorbital canal posterior to the parietal
which is located along the midline just in front of
branch of the latter (for discussion on os
the ascending wings, is deep and well developed
dermosphenoticum see, e.g. Harrington, 1955 and
(Fig. 2, vkp).
Bogutskaya, 1989).
Sclerotic bones, a pair of small dish-shaped bones
Os pterosphenoideum [os pleurosphenoideum; os
that cap the anterior and posterior margin of the
alisphenoideum]. The pterosphenoid [also called
eyeball. They are weakly calcified in G. ternetzi.
pleurosphenoid or alisphenoid but these bones in
mammals and reptiles respectively are not homolo-
Sphenoid region (Figs 1, 2), cranium bones
gous] is a paired bone which develops from the
which together form the floor and sidewalls of the
taenia marginalis posterior; this cartilage bar (bilat-
middle part of the neurocranium.
erally paired) is first visible as an anterior extension
Os orbitosphenoideum. The orbitosphenoid is a of the auditory capsule. It grows anteriorly toward
large median unpaired cartilage bone consisting of the middle of the orbit where it is connected to its
two diverging plates. The orbitosphenoid develops counterpart on the other side by the epiphyseal bar.
from the taenia marginalis anterior and forms the
ZOOSYST. ROSSICA Vol. 17 • N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi 117
The pterosphenoid forms the posterior upper re- upward and forward over the epiotic along the pos-
gion of the orbit. Internally the pterosphenoid con- teriorventral edge of the parietal, the lower, smaller
stitutes a part of the base for the arch of the process extending inward toward the opisthotic to
epiphyseal bar. Laterally the pterosphenoid is bor- which it is attached by a ligament. The posttemporal
dered by the frontal, posteriorly by the sphenotic, carries the main laterosensory canal also called the
ventrally by the prootic, and anteriorly by the orbi- posttemporal canal.
tosphenoid. The foramen for the trochlear nerve is
relatively large and located between the frontal and Os sphenoticum [os autosphenoticum]. The sphe-
dorsal parts of the margins of the pterosphenoid and notic bone is a paired chondral ossification that
the orbitosphenoid. develops from the taenia marginalis posterior and
the tectum synoticum (an unpaired thin dorsal sheet
Otic region [cranial vault] (Figs 1, 2). It is mostly of cartilage that partially covers the posterior chon-
formed from capsula auditiva (auditory, or otic, drocranium).
capsule) that is a cartilaginous skeleton about the The sphenotic lies below the frontals and the up-
inner ear in Elasmobranchii or a chondral skeleton per portions of the pterotics that contain the sensory
in bony fishes comprised of the prootic, opisthotic canals. The frontal and pterotic overlaps the sphe-
(or its replacement), intercalar, epiotic, exoccipital, notic to a certain extent forming the dilator fossa.
sphenotic, pterosphenoid and basisphenoid as walls The dilator fossa is formed mainly from the sphe-
and floor with the parietals as the roof. notic and provides the surface of origin for the dila-
Os parietale. The parietal bone is a paired dermal tor operculi muscle. Laterally the sphenotic has a
bone that covers the hind part of the cranium, over- strong spinous process, directed almost ventrally
lapping the dorsal edge of the sphenotic, pterotic, rather than laterally (Fig. 2, spho). The levator arcus
epiotic and the anterior edge of the supraoccipital. palatine muscle arises from the posterior surface of
The parietals are overlapped anteriormedially by the the sphenotic spine.
frontals.
The two rather narrow parietals in G. ternetzi are Os pteroticum. The pterotic consists of both carti-
sheets of bone that do not meet along the midline, laginous (autopterotic) and intramembranous (su-
but are separated by the large posterior (postpineal) pratemporal-intertemporal, or dermopterotic) com-
fontanel (the posterior part of the large dorsomedial ponents. The autopterotic is developed from the otic
cranial fontanel). A posterior branch of the capsule and encloses the horizontal semicircular
supraorbital sensory canal system passes backward canal of the inner ear. The neurodermal component
in the median part of the frontal continuing through is represented by the canal that connects the frontal
the parietal as the parietal sensory canal and opens canal and the extrascapular canal and receives the
to the exterior over the supratemporal canal. Thus, mandibular-preopercular canal from the suprapre-
the very end of the supraorbital canal tube almost or opercle (Fig. 4, pto).
completely overlaps the supratemporal canal tube Dorsally the pterotic is overlaid by the respective
but does not communicate with the latter. parietal and frontal. Anteriorly the pterotic contacts
the sphenotic, ventromedially the prootic, pos-
Os extrascapulare [extrascapula; os tabulare; os teroventrally the exoccipital and posteriorly the
supratemporale] (Figs 2, 4, esc). The extrascapular epiotic. The prootic, sphenotic, exoccipital and
[tabular, supratemporal, or scale bone] is a paired epiotic joints of the pterotic are synchondral, and the
dermal bone that contacts the parietal at the lower parietal and opisthotic are syndesmotic joints
posterior region where the supratemporal sensory (Weitzman, 1962). The anteroventral surface is
canal leaves the parietal. At the same time, the ex- grooved by the rear portion of the hyomandibular
trascapula receives the sensory canal from the fossa. There is no foramen between the sphenotic
pterotic bone being a place of the interconnection of and pterotic.
the two main canals of the posterior part of the head
into a single canal that goes further caudad into the Os prooticum. The prootic is a paired chodral
posttemporal bone. bone developed from the otic capsule and the para-
chordal cartilage (a rod-shaped paired cartilage on
Os posttemporale [suprascapula, suprascapular, either side of the notochord; paired cartilages unite,
supracleithrum I] (Fig. 1, ptt). The posttemporal is a forming the base of the chondrocranium and are
paired superficial dermal bone that attaches the replaced by the prootic bones).
pectoral girdle to the skull. The posttemporal bone The prooticum is an extensive bone of the com-
is treated by some (e.g. Weitzman, 1962) as a part plicated structure that lies between the parasphe-
of the pectoral girdle. noid, prootic of the other side, the basioccipital,
It is attched to the neurocranium via two projec- exoccipital, pterotic and sphenotic. The bone is
tions, or processes, the upper pointed one extending pierced by foramina that accommodate branches of
118 N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi • ZOOSYST. ROSSICA Vol. 17
the trigeminal and facial nerves. The auditory fora- cartilage and parachordal cartilage. It bears a large
men as seen from the lateral view is the largest one foramen (lateral occipital foramen), contacts the
and extends along the most part of the lateral sur- supraoccipital dorsally, the epiotic laterally and the
face of the prootic.The subtemporal fossa is a very basioccipital ventrally, forms the posterior hind
shallow depression in the posterior region of the margin of the cranium and borders the lateral and
suture between the prootic, pterotic, and basioccipi- posterior margins of the foramen magnum.
tal. Internally and externally the exoccipital forms the
dorsal portion of the bony lagenar capsule. Just
Os epioticum [os epioccipitale]. The epiotic above the lagenar capsule is a large foramen for the
[epioccipital] bone is a paired chondral bone devel- tenth cranial (vagus) nerve. Just anterior to this fo-
oped from the otic capsule and situated on the poste- ramen are few small and minute foramina. Through
rior surface of the neurocranium. It encloses the the largest of these (though it is very small relative
posterior semicircular canal of the inner ear. to the foramen for the tenth nerve) passes the ninth
The epiotic contacts the supraoccipital and parie- cranial (glossopharyngeal) nerve.
tal dorsally, and the exoccipital ventrally. The lower
anterior region of the epiotic contacts the pterotic, Os basioccipitale. The basioccipital is a median
while a process of the epiotic extends to contact the unpaired chondral bone that develops from the
parietal above and the pterotic below. This epiotic parachordal cartilages. It contacts the prootics ante-
process that bridges the posttemporal fossa is very riorly, the parasphenoid ventromedially, and the
narrow in G. ternetzi. Ascin most characins, the exoccipitals dorsally, and forms the posteroventral
posttemporal fossae are well developed, being actu- hind margin of the cranium, articulating with the
ally fontanels, the deepest part covered by a strong centrum of the first vertebra.
membrane for the origin of epaxial muscles. The lower anterior portion of the basioccipital is
divided into two bilateral lamellae of bone that con-
Os intercalare [os opistoticum]. The intercalar tact the two posterior processes of the parasphenoid
bone [intercalary; opistotic] is a small membrane below. Between the bony lamellae formed by the
bone that may be homologous with a cartilage bone prootics and basioccipital, above the parasphenoid,
in more basal fishes (Patterson, 1977). and between the bilateral posterior projections of the
The intercalary is very thin and poorly ossified in parasphenoid, lies the large posterior myodome.
G. ternetzi; it is located on the surface in the region The myodome is open (“floorless” sensu Weitzman,
of the suture between the prootic, pterotic and the 1962) posteriorly.
exoccipital and associated with the ventral process
of the posttemporal. Cranium: splanchnocranium (viscerocranium)
(Figs 4, 5).
Occipital region (Figs 1, 2).
Os supraoccipitale. The supraoccipital bone is of Mandibular arch (jaw, jaw cartilage, oral jaw
a mixed origin. The main body of the bone is a skeleton, pharyngeal arch 1 skeleton, visceral arch
chondral ossification that develops from the tectum 1): skeletal and cartilagenous elements of the first
synoticum (an unpaired thin dorsal sheet of cartilage pharyngeal arch. The manibular arch is subdivided
that partially covers the posterior chondrocranium). into the dorsal part (palatoquadrate arch, dorsal
It is large constituting the postero-dorso-median visceral arch 2, upper jaw or upper pharyngeal jaw)
surface of the cranial roof. It bears an enlarged, and the ventral part (ventral mandibular arch, or
posteriorly pointed, triangular process commonly lower jaw). In a specimen of 4.2 mm NL the metap-
called the supraoccipital crest that extends postero- terygoid and symplectic are slightly ossified while
dorsally; the crest is an ossification of the connec- the ectopterygoid, entopterygoid and qudrate start to
tive median septum separating the anterior trunk progressively calcify since 5.5 mm NL. The only
muscles. bone which appears much later is the palatine (in
The supraoccipital is considerable notched along specimens since 7.2-8.6 mm SL). A very late ossifi-
the medial anterior margin forming the posterior cation of the palatine was also found in Brycon
edge of the postpineal foramen (posterior part of the moorei (Vandewalle et al., 2005).
dorsal cranial fontanel). Laterally and anteriorly it Os palatinum [os palatine]. The palatine [palatal]
sends an arch under the posterior median portion of bone is a paired chondral bone on the roof of the
the parietal. The supraoccipital crest is well devel- mouth lateral to the vomer that may properly be
oped extending upward and caudad relative to the called os autopalatinum (the autopalatine) that de-
posterior cranial surface (Figs 1, 2, so). rives from the pars autopalatine of the palatoquad-
rate cartilage but apparently in characiforms lacks
Os exoccipitale. The exoccipital is a paired the dermal component (os dermopalatinum), which
chondral bone that develops from the occipital arch is often dentigerous in higher teleosteans.
ZOOSYST. ROSSICA Vol. 17 • N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi 119
In G. ternetzi the autopalatine is a toothless dorso- ticulating with the lateral extremity of the premax-
ventrally depressed sand-glass-like bone slightly illa. The body of the maxillar blow the joint is elon-
elongated anteroposteriorly (Fig. 4, pl). Its anterior gated and oval-shaped. In general, the maxillar is
end bears a deep articulatory surface that is attached not long. The posterior tip of the maxillary does not
with the anterolateral margin of the vomer. In two extend to the posterior border of the second
cases, one of the two lamellae forming the articula- infraorbital.
tory facet is penetrated by a very small foramen
though in most cases the autopalatine is not fenes- Os praemaxillare. The premaxilla [premaxillary
trate. If present, the foramen is much smaller than bone] is a paired dermal bone that forms a proximal
that shown in Bryconamericus by Serra & Langeani part of the upper jaw.
(2006). The premaxilla is a very thick L-like heavy bone.
The premaxilla is immovably joined to its counter-
Os ectopterygoideum. The ectopterygoid is a part and to the ethmoid behind by very short liga-
paired dermal bone located at the anterior part of the ments. Its lateral limb is almost equal to the vertical
palatoquadrate. limb [premaxilla ascending process]. The ascending
In adults G. ternetzi it is a long thin bone that is process fits into a groove on the dorsolateral surface
very narrow anteriorly where it meets the auto- of the ethmoid. The premaxillar bears two rows of
palatine and slightly wider at its posterior synostosis teeth along the anterior edge. The outer row has 4-6
with the quadrate. tricuspid teeth which are slightly smalle than teeth
of the inner row. The teeth in the inner row are
Os entopterygoideum [os endopterygoideum; os commonly five, tricuspid, the second one (from the
mesopterygoideum]. The entopterygoid is a paired midline) is the largest and the most lateral teeth is
dermal bone that forms the anteroventral and ventral the smallest.
surface of the orbit. It develops in the membrane
dorsomedial to the palatoquadrate cartilage. Ventral mandibular arch (lower part of man-
In G. ternetzi it is roughly triangular, with its pos- dibular arch, lower jaw, mandible, mandibular se-
teroventral margin almost straight (Fig 4, entpt). ries): the ventral portion of the first pharyngeal arch,
comprising the lower jaw.
Os metapterygoideum. The metapterygoid is a Since Haines (1937), Lekander (1949) and Har-
chodral bone that develops from the palatoquadrate rington (1955) the terminology used for the bones of
cartilage. The posterior edge of the metapterygoid the lower jaw of the teleosts seems to be settled as
meets by means of cartilage the dorsoposterior sur- given below.
face of the symplectic and the lower anterior portion Os dentale. Lekander (1949) found that the den-
of the hyomandibular. The anterior edge of the tary bone (dental bone) in Phoxinus phoxinus (Cy-
metapterygoid meets by means of cartilage the prinidae) is formed from several primordia and is of
quadrate and overlaps the entopterygoid. both dermal and endochondral origin. However it is
As is typical for characids, the metapterygoid and still not clear if a chondral element takes any part in
the quadrate, and, to a much lesser degree, the sym- the formation of the dentary. It forms the antero-
plectic form the borders of a large, central circular lateral part of the lower jaw and develops outside
foramen (Fig. 4.). from the Meckel’s cartilage appearing first at the
anterior part of the latter; it is apparently formed by
Os quadratum. The quadrate bone is a chondral a membranodermal component and a neurodermal
bone that develops from the palatoquadrate carti- component that develops into a sensory mandibular
lage. The body of the quadrate ossifies first at the canal. In the adult, the dentary meets its counterpart
ball-and-socket articulation with the anguloarticular anteriorly at the mandibular symphysis. The dentary
(Fig. 5). abuts the retroarticular posteriorly, and surrounds
the anguloarticular.
In adult G. ternetzi the quadrate has a markedly
concave dorsal margin to form the border of the In G. ternetzi the dentary completely lacks the
foramen and a very poorly pronounced posterior coronoid process. The sensory canal goes along the
process that is represented by a deep rounded struc- whole lower margin of the bone, well ossified, and
ture not elongated or pointed. commonly consists of five segments (Fig. 5, d, dc).
In adults the dentary bears four large teeth, the sec-
ond one (from the midline) being the largest. The
Os maxillare. The maxilla [maxillary bone] is a
teeth have commonly five cusps, the lower ones
paired dermal bone that forms a distal part of the
being very small. Posterior to the last large tooth is a
upper jaw.
series (3-4) of small unicuspid teeth. In smaller
In G. ternetzi the maxillar is toothless. Its upper
specimens (as the specimen figured) the size differ-
arm moves at the lateral portion of the premaxilla.
ence between the large teeth and small teeth is not
Just at the of the upper arm is a small facet for ar-
120 N.G. Bogutskaya et al.: Osteology of Gymnocorymbus ternetzi • ZOOSYST. ROSSICA Vol. 17
so marked and the transition from large teeth to riorly and abuts the ventral shelf of the dentary ante-
small teeth is more gradual than in large specimens. riorly.
The symphysis of the lower jaw consists of three
convoluted bony folds. The folds on one side fit into Pharyngeal arch 2 skeleton (arcus hyoideus).
the spaces formed by the folds of the other side as The hyoid arch, or bar, is the arch lying between the
described by Weitzman (1962). jaws and gill arches, with which it is believed ho-
mologous and which helps support the floor of the
Os angulo-articulare [os articular]. The anguloar- mouth cavity. It is subdivided into the dorsal part
ticular, together with the dentary, coronomeckelian, (dorsal hyoid arch) and the ventral part (ventral
retroarticular and Meckel’s cartilage, constitute the hyoid arch) and composed of the paired exo- and
mandible. It is a paired bone of a mixed (com- endoskeleton elements.
pound) origin that results of the fusion of the dermal The dorsal hyoid arch (dorsal visceral arch 2) is
angular and the cartilaginous articular. The angular a part of pharyngeal arch 2 skeleton and suspensor-
part ossifies initially on the posterolateral surface of ium at the same time. It includes the opercular se-
Meckel's cartilage near the articulation with the ries, hyomandibular, and symplectic.
quadrate (Vandewalle et al., 2005; our data). Pos-
teroventrally, the anguloarticular is ligamenttously Opercular series (gill cover; opercular flap; oper-
connected to both the interopercular bone and the cular apparatus) (Fig. 4). All four bones of the oper-
posterior ceratohyal. The posterior end of the articu- cular series are already partly ossified in the smallest
lar bears a socket for the condylar surface of the specimens (4.0 mm of notochord length, 9 days
quadrate. A segment of the canal on the anguloar- after hatching).
ticular is located just below the articular surface Os praeoperculum [os praeoperculare]. The pre-
being a continuation of the canal on the dentary onto opercle [preopercular bone] is a paired dermal bone
the preopercle (Fig. 5, aart, aartc). which lies in front of the gill cover and which bears
the upper part of the preoperculo-mandibular sen-
Cartilago Meckeli. The Meckel’s cartilage [cera- sory canal.
tomandibular cartilage, also called mandibular carti- It is clearly L-shaped with the preopercle horizon-
lage or primary mandible], the embryonic lower jaw tal limb (the lower, horizontal portion of the preop-
of bony fishes which ossifies in a number of bones ercle bone) and the preopercle vertical limb (the
different in different groups of fishes. In lower upper, vertical portion of the preopercle bone). The
teleosts, it ossifies at least in part as the anterior end of the preopercle fits into a groove on
coronomeckelian, articular and retroarticular. It the median lower region of the quadrate, while the
remains in some adult fishes, including characids, as dorsal end lies between the infraorbital bones and
a pointed rod embedded in the dentary and angu- the opercle. The upper end of the preopercle does
loarticular. The Meckel's cartilage extends along the not fuse to the suprapreopercle.
floor of the median mandibular fossa. Part of the
median face of the coronomeckelian bone is in con-
Os suprapraeoperculum [os supraoperculum].
tact with Meckel' s cartilage.
The suprapreopercle is a dermal bone located right
above the upper end of the preopercle.
Os coronomeckeli [sesamoid angular, supraangu- The suprapreopercle is a long tubular bone repre-
lar, sesamoid articular, articular sesamoid, splenial, sented by a neurodermal component and completely
os meckeli or d bone]. The corono-meckelian bone lacking any membranodermal component (Fig. 4,
is one of the derivates of the Meckel’s cartilage. spop). It is not fused to the preopercle even in the
It is a small round bone lodged in the medial in- adult specimens examined.
ner surface of the anguloarticular just at the level of
the dentary margin (Fig. 5, cm). Posterodorsally it
Os operculum [os operculare]. The opercle [oper-
bears a crest for attachment of a portion of the ad-
cular bone] is a paired dermal bone that is the prin-
ductor mandibulae muscle.
ciple and largest component of the gill cover com-
Os retroarticular [angular, Bridge's ossicle a, prising its upper part.
lower articular or angulo-retroarticular]. The retroar-
The opercle is a fairly deep, smooth bone on the
ticular is a paired cartilage bone that forms at the
lateral part of the face and below the posterior re-
posteroventral tip of Meckel's cartilage where the
gion of the hyomandibular. It forms a ball-and-
interoperculomandibular ligament attaches.
socket joint with the hyomandibular that is located
It is small, roughly triangular in shape, and lo- at the anterior margin of the bone about one third of
cated at the very posteroventral end of the lower jaw the bone depth below its upper margin.
(Fig. 5, rart). The retroarticular is ligamentously
connected to the interopercle and preopercle poste-
