ZOOLOGIA 28 (1): 97–111, February, 2011
doi: 10.1590/S1984-46702011000100014
Morphological description of Dipturus mennii (Chondrichthyes:
Elasmobranchii: Rajidae) and its differentiation from Dipturus trachyderma
Renan A. Moreira1; Ulisses L. Gomes1, 3 & Marcelo R. de Carvalho2
1
Laboratório de Taxonomia de Elasmobrânquios, Departamento de Zoologia, Instituto de Biologia, Universidade do Estado
do Rio de Janeiro. Rua São Francisco Xavier 524, 20559-900 Rio de Janeiro, RJ, Brazil.
2
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo. Rua do Matão, Travessa 14, 101,
05508-900 São Paulo, SP, Brazil.
3
Corresponding author. E-mail: ulisses@uerj.br
ABSTRACT. Squamation patterns and skeletal anatomy (neurocranium, visceral arches, synarcual cartilage, scapulocoracoid,
puboischiadic bar, and mixopterigium) of Dipturus mennii Gomes & Paragó, 2001 are described as a contribution to our
limited knowledge of the anatomy of species of Dipturus Rafinesque, 1810. The hyoid and branchial arches, as well as
the synarcual cartilage, are described for the first time in this species. We provide morphological comparisons of this
species with Dipturus trachyderma (Krefft & Stehmann, 1975), a species that may be confused with D. mennii; we further
corroborate, through anatomical features, that these species warrant separate taxonomic recognition. The main differences between D. mennii and D. trachyderma were found in squamation of the nuchal and middisc region, neurocranium, pectoral girdle, and principally the clasper skeleton. The morphology of the pelvic girdle is similar in both species.
Dipturus is characterized by having the ventral terminal cartilage J-shaped (as opposed to the Z-shaped ventral terminal
cartilage in Zearaja, whose species were, until recently, placed in Dipturus). Additional characters that may be derived
for Dipturus include the anterior rostral groove and elevated rostral proportions.
KEY WORDS. Rajinae; skates; southwestern Atlantic Ocean; taxonomy.
Skates (Rajidae) of the genus Dipturus Rafinesque, 1810
are distributed worldwide and have their greatest diversity in
the continental slope but are also present in deeper areas of
the continental shelf (MCEACHRAN & MIYAKE 1990a, b, EBERT &
COMPAGNO 2007, LAST et al. 2008). Dipturus is presently composed of some 42 valid species (SÉRET 1989, COMPAGNO 1999,
2005, LAST 2008, LAST et al. 2008, SÉRET & LAST 2008), with several new species awaiting description. However, many species
of this genus remain poorly known and require further morphological and taxonomic scrutiny, efforts typically constrained
by their conservative morphology and lack of adequate material for detailed comparisons. There are few comprehensive
taxonomic studies of Dipturus (ISHIYAMA 1958, STEHMANN 1970,
HULLEY 1972, L AST et al. 2008).
Species of Dipturus from the southwestern Atlantic Ocean
have been little studied morphologically and taxonomically in
comparison to other rajid genera from this region (e.g. KREFFT
1968, KREFFT & STEHMANN 1974, MENNI 1971, 1972a, b, 1973,
SADOWSKY & MENNI 1974, FIGUEIREDO 1977, MCEACHRAN 1982, 1983,
GOMES & PARAGÓ 2005, CARVALHO et al. 2005, 2006). Five species
are presently recognized as valid from the southwestern Atlantic: Dipturus teevani (Bigelow & Schroeder, 1951), D. leptocauda
(Krefft & Stehmann, 1975), D. trachyderma (Krefft & Stehmann,
1975), D. mennii Gomes & Paragó, 2001 (Dipturus diehli Soto &
Mincarone, 2001 is a junior synonym), and D. argentinensis
Astarloa, Mabragaña, Hanner & Figueroa, 2008. Dipturus
chilensis (Guichenot, 1848), which also occurs in the southwestern Atlantic, was transferred to Zearaja Whitley, 1939 by
LAST & GLEDHILL (2007) in their resurrection of this genus. Additional Dipturus species that occur in the Gulf of Mexico or off
northern South America (MCEACHRAN & CARVALHO 2002), and
which may eventually be recorded farther south, include D.
garricki (Bigelow & Schroeder, 1958), D. oregoni (Bigelow &
Schroeder, 1958), D. bullisi (Bigelow & Schroeder, 1962), and
D. olseni (Bigelow & Schroeder, 1951).
Dipturus trachyderma was originally described from off
southern Argentina from a single specimen (KREFFT & STEHMANN
1975; see also MENNI & GOSZTONYI 1977, MENNI & STEHMANN 2000).
Subsequently, LEIBLE & STEHMANN (1987) recorded D. trachyderma
off Chile and described its mixopterigium, neurocranium,
scapulocoracoid, and pelvic girdle. There are no reliable records
of D. trachyderma from Brazil; note that D. trachyderma of GOMES
& PICADO (2001) is, in part, D. mennii. Dipturus mennii was described from adults and juveniles that were previously identi-
© 2011 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | All rights reserved.
98
R. A. Moreira et al.
fied as D. trachyderma and collected from off the states of Rio
Grande do Sul to Rio de Janeiro (GOMES & PARAGÓ 2001). The
taxonomic separation of D. menni from D. trachyderma is not
straightforward; both species are similar and may be easily confused. According to GOMES & PARAGÓ (2001) dorsal squamation
patterns are of great importance in distinguishing both species, a claim that requires further corroboration.
The aim of the present paper is to morphologically describe Dipturus mennii, specifically its squamation patterns, neurocranium, branchial arches, synarcual cartilage, scapulocoracoid, pelvic girdle, and mixopterygial skeleton. By doing so,
we hope to improve our understanding of the taxonomy and
morphology of southwestern Atlantic species of Dipturus, further corroborating the taxonomic separation between D. mennii
and D. trachyderma.
MATERIAL AND METHODS
Studied specimens belong to the ichthyological (UERJ)
and anatomical (A. UERJ) collections of the Department of
Zoology of the Universidade do Estado do Rio de Janeiro. Two
specimens (UERJ 2106, UERJ 1893) were intact prior to our
study, but three (UERJ 2103, UERJ 2104, UERJ 2105) were represented only by the head and pelvic girdle, thus not all measurements and counts were recorded. Some skeletal components were hot-water macerated with added potassium carbonate to facilitate the release of flesh. Some dry skeletal components were prepared with dermestid beetles, which facilitated the observation of minute neurocranial foramina. The
initials TL and DW represent, respectively, total length and
disc width.
Meristic data and external measurements were taken from
LEIBLE & STEHMANN (1987), GOMES & PICADO (2001), and GOMES &
PARAGÓ (2001). Measurements are presented in Table I. External morphological descriptions were based on KREFFT & STEHMANN
(1975) and LEIBLE & STEHMANN (1987). The description of the
pectoral and pelvic girdles followed LEIBLE (1988). Mixopterygia
were described following STEHMANN (1970), HULLEY (1972), and
LEIBLE (1988). Gill arches were described based on EL-TOUBI &
HAMDY (1959). The description of neurocranium followed EL-
Table I. Measurements (in millimeters and percentages of total length, when available) taken from specimens of D. mennii; all specimens
are from the UERJ collection.
Specimen number
Measurements
Total length
2103 (male)
2104 (female)
2105 (female)
mm
1893 (male)
%
mm
mm
mm
mm
2106 (male)
%
950
100.00
–
–
–
1544
100.00
Disc width
734
77.26
–
–
–
1100
71.20
Disc length
575
60.50
–
–
–
870
7.50
Preorbital length
203
21.40
280
362
80
310
20.10
Preoral length
217
22.80
285
380
390
305
19.75
Prenasal length
179
18.80
260
320
335
260
16.80
Head length
335
35.30
479
580
580
523
33.90
Mouth width
80
8.40
133
155
140
122
7.90
Internasal length
83
8.70
120
140
135
123
8.00
1st branchial slit width
14
1.50
16
10
20
15
1.00
11
1.20
17
20
17
10
0.60
Distance between 1st branchial slits
5th branchial slit idth
142
14.94
210
260
245
215
13.90
Distance between 5th branchial slits
90
9.50
120
170
162
143
9.30
1st dorsal fin height
27
2.80
45
–
45
40
2.60
Length of 1st dorsal fin
45
4.70
70
–
65
70
4.50
2nd dorsal fin height
25
2.60
45
–
43
35
2.30
38
4.00
–
–
60
62
4.00
382
40.20
–
–
610
660
42.70
2nd dorsal fin length
Caudal length
Clasper outer length
33
3.47
190
–
–
195
12.60
Clasper inner length
50
5.26
277
–
–
305
19.70
ZOOLOGIA 28 (1): 97–111, February, 2011
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
TOUBI & HAMDY (1959), HULLEY (1972), LEIBLE & STEHMANN (1987),
LEIBLE (1987, 1988), and COMPAGNO (1988). Neurocranial measurements were based on HUBBS & ISHIYAMA (1968). The synarcual
cartilage was described following GOMES et al. (1997).
Anatomically prepared material of Dipturus mennii is the
following: UERJ 1893 (paratype), male, 961 mm TL, 763 mm
DW, southern Rio Grande do Sul state, 1996; A.UERJ 1006, sex
unknown, TL and DW undetermined, southern Rio Grande do
Sul state; A.UERJ 1007, sex unknown, TL and DW undetermined, southern Rio Grande do Sul state; A.UERJ 1008, male,
TL and DW undetermined, southern Rio Grande do Sul state;
UERJ 2103, male, TL and DW undetermined, Paranaguá (Paraná
state); UERJ 2104, female, TL and DW undetermined, Paranaguá
(Paraná state); UERJ 2105, female, TL and DW undetermined,
Paranaguá (Paraná state); UERJ 2106, male, 1544 mm TL, 1100
mm DW, Paranaguá (Paraná state). Other material consulted
for the present paper is listed in GOMES & PARAGÓ (2001), GOMES
& PICADO (2001), and GOMES & COSTA (2003).
99
TAXONOMY
Dipturus mennii Gomes & Paragó, 2001
Morphological description
Squamation. Both dorsal (Figs 1 and 2) and ventral (Fig.
3) sides are relatively smooth, with only the interbranchial region slightly rough due to the presence of minute dermal denticles that are not visible to the naked eye and hardly sensitive
to the touch. The tip of the rostrum is covered with coarse
thorns, and the dorsal interorbital region is rough with very
small dermal denticles that do not form a specific pattern (Fig.
2). Orbital thorns vary from six to 12 and contour the orbits,
making it difficult to distinguish antorbital from interorbital
thorns. No postorbital thorns are present (Fig. 2). There are
two to seven spiracular thorns, five to seven nuchal thorns,
one to four suprascapular thorns that may vary in the same
specimen, and there is a single continuous row of 18 to 25
2
1
3
Figures 1-3. Dipturus mennii, UERJ 2106: (1) dorsal view; (2) interorbital region; (3) mouth and interbranchial region. Scale bars:
1 = 200 mm, 2 = 50 mm, 3 = 100 mm.
ZOOLOGIA 28 (1): 97–111, February, 2011
100
R. A. Moreira et al.
neurocranial measurements). A narrow rostral appendix (RA) is
present and is much less calcified than the rostrum. The rostral
appendix is perforated by a series of small rostral appendix foramina (new term) (RAF) (Fig. 4) for the passage of the superficial ophthalmic branches of the trigeminal-facial nerves (V + VII).
The anterior fontanelle (AF) is elongated and oval, presenting
two regions, the anterior precerebral portion (above the rostrum)
and the posterior supracranial portion (above the skull roof).
The anterior margin of the precerebral fontanelle is not clearly
defined due to a narrow anterior rostral groove (RG) that extends in anteriorly toward the rostral apex. The limit of the anterior groove and the anterior fontanelle is marked by the pres-
mediodorsal thorns (Tabs II and III). The sexually mature male
examined presented 56 alar thorns on the left side and 53 on
the right, arranged in three distinct rows. In the caudal region,
the males present three rows of thorns and females have five.
The mediocaudal row is composed of 25 to 43 thorns, the
laterocaudal thorns vary from six to 24 on the left side and
from seven to 26 on the right side; laterocaudal thorns do not
reach the tail end. The second row of laterocaudal thorns
(semilateral thorns) in females has 8 thorns on each side. The
interdorsal space presents one to three thorns (Tab. II).
Neurocranium. Dipturus mennii presents a long and stout
rostrum (R) (almost 66% of neurocranial TL; see Table IV for
Table II. Thorn counts in specimens of D. mennii (R = right, L = left); all five specimens are from the UERJ collection.
Male
Nuchal
Suprascapular
Mediodorsal
Female
1893
2103
2106
2104
2105
5
5
7
5
6
L = 2/R = 2
L = 4/R = 2
L = 4/R = 3
L = 1/R = 1
L = 3/R = 4
18
–
25
–
–
Caudal row
3
3
3
5
5
Mediocaudal
25
29
43
–
30
L = 6/R = 7
L = 11/R = 11
L = 14/R = 12
–
L = 24/R = 26
–
–
–
–
L = 8/R = 8
Lateral caudal rows
Semilateral caudal rows
Interdorsals
1
2
3
–
3
Alar
–
–
L = 56/R = 53
–
–
Orbital
L = 6/R = 7
L = 8/R = 7
L = 12/R = 10
L = 11/R = 11
L = 11/R = 10
Spiracular
L = 2/R = 3
L = 4/R = 4
L = 4/R = 7
L = 4/R = 4
L = 6/R = 5
Table III. Comparison of thorn counts in specimens of D. mennii and D. trachyderma. (R) Right, (L) left.
Dipturus mennii
Male
Nuchal
Suprascapular
Mediodorsal
Dipturus trachyderma *
Female
Male
Female
5-7
5-6
0
0
L = 2-4 / R = 2-3
L = 1-3 / R = 1-4
0
0
18-25
–
0
0
Caudal row
3
5
3
5
Mediocaudal
25-43
30
24-43
24-24
L = 6-14 / R = 7-12
L = 24/26
L = 4-26
L = 20-30
–
L=8/R=8
–
L = 14-30
Lateral caudal rows
Semilateral caudal rows
Interdorsal
1-3
3
0-4
1-3
L = 56 / R = 53
0
L = 46 / R = 48
0
L = 6-12 / R = 7-10
L = 11 / R = 10-11
L = 0-12 / R = 0-12
L = 0-7 / R = 0-7
L = 2-4 / R = 3-7
L = 4-6 / R = 4-5
0
0
Alar
Orbital
Spiracular
* Data from LEIBLE & STEHMANN (1987).
ZOOLOGIA 28 (1): 97–111, February, 2011
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
101
4
5
6
7
Figures 4-7. Neurocranium of D. mennii (UERJ 2104), in dorsal (4), ventral (5), lateral (6), and occipital (7) views. (ACV) anterior cerebral
vein foramen, (AF) anterior fontanelle, (ANC) antorbital condyle, (AON) antorbital foramen, (AOPF) anterior ophthalmic foramen, (APA)
afferent pseudobranchial artery foramen, (ASC) anterior semicircular canal, (ICF) internal carotid foramen, (EB) epiphysial bridge, (EPH)
endolymphatic foramen, (FH) facet for hyomandibular cartilage, (FM) foramen magnum, (RG) rostral groove, (Hm VII) hyomandibular
branch foramen, (IOF) internal orbital foramen, (JA) jugal arch, (LSC) lateral semicircular canal, (LFX) lateral foramen of the vagus nerve,
(NC) nasal capsule, (OC) orbitonasal canal, (OCC) occipital condyle, (OP) ophthalmic process, (OS) optic stalk, (PCV) posterior cerebral
vein foramen, (PF) posterior fontanelle, (PFS) parietal fossa, (PHF) perilymphatic foramen, (POF) prootic foramen, (PON) posterior
orbitonasal foramen, (POP) postorbital process, (POPF) posterior ophthalmic foramen, (PRO) preorbital process, (PSC) posterior semicircular canal, (PTC) pterotic crest, (PTP) pterotic process, (R) rostrum, (RA) rostral appendix, (RAF) rostral appendix foramen, (RF)
rostral foramen, (SC) supraorbital crest, (SOF) supraophthalmic foramen, (II) optic nerve foramen, (III) oculomotor nerve foramen, (IV)
trochlear nerve foramen, (IX) glossopharyngeal nerve foramen, (X) vagus nerve foramen. Scale bars: 4-5 = 40 mm, 6-7 = 30 mm.
ZOOLOGIA 28 (1): 97–111, February, 2011
102
R. A. Moreira et al.
Table IV. Neurocranial measurements (mm) taken from specimens of D. mennii. Percentages are in relation to neurocranial total length;
all specimens are from the UERJ collection.
Specimen number
Measurements
Neurocranium length
Nasobasal length
Rostral cartilage length
Neurocranium width
1006
1008
2104
mm
mm
%
mm
%
–
385
100.00
480
100.00
130
145
37.70
165
34.40
–
240
62.30
320
66.70
135
17
4.40
–
–
Interorbital width
55
66
17.10
78
16.25
Rostral base width
40
55
14.28
72
15.00
Anterior fontanelle width
–
22
5.70
31
6.40
Epiphysial bridge width
–
6
1.50
8
1.60
Posterior fontanelle length
–
60
15.60
71
14.80
Rostral appendix length
–
–
–
91
18.90
Appendix length width
–
–
–
10
2.10
Width between optic capsules
74
87
22.30
98
20.40
Basal plate width
45
52
13.50
62
12.90
Nasal openings width
–
32
8.30
33
6.90
Internasal width
45
48
12.50
60
12.50
ence of a small rostral foramen (new term) (RF). There is a narrow epiphysial bridge (EB) separating the anterior fontanelle from
the posterior fontanelle (PF), which is completely supracranial
and proportionally smaller and less oval than the anterior fontanelle (Fig. 4). At the anterior extremity of the neurocranial
roof there is the posterior margin of the anterior fontanelle. Ventrally, the neurocranial basal plate is narrow anteriorly between
the nasal capsules, but becomes wider posteriorly (Fig. 5). In the
center of the basal plate is the foramen for the passage of the
internal carotid artery (ICF) (Fig. 5), which may have two openings or may lie within a depression which contains both openings (more specimens should be observed in order to check the
state of this character). The nasal capsule (NC) is somewhat rectangular and anteriorly arched (Fig. 4). At the junction of the
nasal capsule with the base of the rostrum is the anterior ophthalmic foramen (AOPF) (Figs 4-6). The anterior ophthalmic foramen is protected by a small protuberance, the ophthalmic
process (OP, new term) (Fig. 4). In D. menni, the anterior ophthalmic foramen has an unusual shape, as it is not completely
enclosed, resembling a groove that opens into the nasal capsule
(Figs 4-6). On the lateral side of the nasal capsule, directed outwardly, there is the antorbital condyle (ANC) that articulates
with the antorbital cartilage. The antorbital cartilage contains a
circular foramen for the passage of a nerve that innervates ampullae of Lorenzini in the anterolatral head region. Dorsally on
the nasal capsule is the well-developed and triangular preorbital
ZOOLOGIA 28 (1): 97–111, February, 2011
process (PRO) that is continuous with the supraorbital crest (SC)
(Fig. 4). The lateral skull roof is dorsally limited by the supraorbital crest pierced by a series of supraophthalmic foramina (SOF)
(Figs 4 and 6) which vary in number among different specimens,
and may even vary between different sides of the same individual; the posterior-most foramina are more developed. Continuous with the crest is the postorbital process (POP), which is
not very pronounced and which limits the posterior roof of the
neurocranium. The orbital region (Fig. 6) is located posterior to
the posterior wall of the nasal capsule, which is pierced by two
foramina, the posterior orbitonasal foramen (PON) and posterior ophthalmic (POPF) foramina. The orbitonasal canal (OC)
follows of the posterior orbitonasal foramen inside the nasal
capsule, opening in anterior orbitonasal foramen (AON). Dorsally to the posterior ophthalmic foramen is the small foramen
for anterior cerebral vein (ACV). Lateral to the posterior
orbitonasal foramen is a large and slightly elliptical foramen for
the optic nerve (II), and almost at the same level but situated
more posteriorly is the large prootic foramen (POF), which is
slightly more rounded than the optic foramen. The hyomandibular branch of the facial nerve (HmVII) is located posteriorly
and slightly more ventrally to the prootic foramen. A small foramen for the internal orbital vein (IOF) is positioned just
anteroventrally to the prootic foramen and slightly dorsal to
the foramen for the afferent pseudobranchial artery (APA), which
is near the ventral limit of the otic capsule. Dorsal to the optic
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
nerve foramen are two small openings for the passage of the
trochlear nerve (IV). Anteroventral to the rather large optic stalk
(OS) is the foramen for the oculomotor nerve (III). The optic
stalk is a flexible and distally flat cartilage situated halfway between the optic nerve and prootic foramina at orbital midlength
(Fig. 6). The otic region may present individual variations in the
configuration of the ridges formed by the anterior (ASC), posterior (PSC) and lateral semicircular canals (LSC) which are more
clearly marked in some specimens. Dorsally, the parietal fossa
(PFS) presents foramina that vary in size and position in each
individual. The perilymphatic foramen (PHF) is always greater
than the endolymphatic foramen (EPH). Delimiting the otic region dorsolaterally is a rounded pterotic process (PTP) (Figs 4
and 5), continuous with a low pterotic crest (PTC) (Figs 4 and 5)
itself weakly visible. The occipital region (Fig. 7) is subrectangular
with a large circular foramen magnum (FM) between the occipital condyles (OCC), which in turn are ventral to two small foramina for the lateral branch of the vagus nerve (LFX). Between
the occipital condyle and the jugal arch (JA) is the vagus nerve
foramen (X), itself below the foramen of the posterior cerebral
vein (PCV). Just below the jugal arch is the glossopharyngeal
nerve foramen (IX).
Synarcual cartilage. The synarcual cartilage is subrectangular, being wider posteriorly at the suprascapulae (SE), followed by the lateral stay (LS) (Figs 8-10). The anterior margin
of the suprascapula is slightly concave and laterally its articular surface is horizontal and broad, parallel to the synarcual
base (Fig. 10). The lateral stay is triangular and widest posteriorly. Anterior to the lateral stay side is a long and subrectangular
anterior lateral flap (ALF) that has a large basal foramen (BF)
medially situated (Figs 8-10). The posterior lateral flap (PLF) is
posterior to the lateral stay but is narrower than the anterior
lateral stay (Fig. 10). The odontoid process (OTP) in the anterior extremity of the synarcual is slightly oval with a prominent odontoid collar (OTC) that completely borders the aperture (Figs 8 and 9). The intermuscular septum is divided into
two regions, anterior and posterior. The anterior intermuscular septum (AIS) extends across the dorsal region of the
synarcual from the odontoid process to the suprascapula. The
posterior intermuscular septum (PIS) continues posteriorly from
the suprascapulae and tapers caudally (Fig. 8). Small, parallel,
dorsal and ventral spinal foramina (DSF and VSF) (Figs 8 and
10) occur throughout almost the entire extent of the lateral
side of the synarcual cartilage. In lateral view these foramina
are covered by the anterior lateral flap and partially by the
posterior lateral flap (Fig. 10).
Hyoid and branchial arches. Dorsally in Dipturus mennii,
the pseudohyoid cartilage (PSH) is situated at the same level,
and placed anteriorly to the five subsequent epibranchials (EP
1-5) (Fig. 11). The epibranchials are subrectangular and similar
in shape (Fig. 11). Slender dorsal extrahyal (DEH) and dorsal
extrabranchial (DEB) cartilages are found external to the
pseudohyoid and each epibranquial element, respectively, ex-
103
8
9
10
Figures 8-10. Synarcual cartilage of D. mennii (UERJ 2104), in dorsal (8), ventral (9), and lateral (10) views. (AIS) anterior intermuscular septum, (ALF) anterior lateral flap, (BF) basal foramen, (DSF)
dorsal spinal foramen, (LE) lateral extension, (LS) lateral stay, (OTC)
odontoid collar, (OTP) odontoid process, (PIS) posterior intermuscular septum, (PLF) posterior lateral flap, (SAS) articular surface
for suprascapula, (SE) suprascapula, (VSF) ventral spinal foramen.
Scale bar: 30 mm.
cept for the fifth epibranchial in which extrabranchials are absent (Fig. 11). Articulated dorsally to each epibranchial are the
posteriorly oriented pharyngobranchials (PHB). The first
pharyngobranchial is triangular. The second and third
pharyngobranchials are similar in size and shape, being elongated and tapering distally. The fourth and fifth pharyngobranchials are fused together along with their respective
epibranchial elements (Fig. 11).In the ventral branchial region,
ceratobranchials 1 to 4 (CB) are similarly shaped (Fig. 12),
whereas ceratobranchial 5 (CB5) is relatively longer and more
slender and articulates with the pectoral girdle posteriorly. The
ZOOLOGIA 28 (1): 97–111, February, 2011
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R. A. Moreira et al.
11
12
Figures 11-12. Branchial arches of D. mennii (UERJ 2104), in dorsal
(11) and ventral (12) views. (BH) basihyal arch, (BB) basibranchial,
(DEB1) dorsal extrabranchial 1, (DEB4) dorsal extrabranchial 4, (DEH)
dorsal extrahyal, (HYB1) hypobranchial 1, (HYB2) hypobranchial 2,
(HYB3) hypobranchial 3, (HYB4) hypobranchial 4, (HYB2?) possible
hypobranchial 2 segment, (EP1) epibranchial 1, (EP5) epibranchial
5, (PHB1) pharyngobranchial 1, (PHB4+5) pharyngobranchial 4+5,
(PSH) pseudohyoid, (VEB4) ventral extrabranchial 4, (VEH) ventral
extrahyal. Extrabranchial elements removed from left side in 11,
and right side in 12. Scale bars: 11= 40 mm,12 =20 mm.
proximal extremity of the first ceratobranchial cartilage is bifurcated, and the longest segment is in contact with the second ceratobranchial cartilage and a cartilage identified as a
possible additional hypobranchial cartilage (HYB2? in Fig. 12).
As in the dorsal elements, each ventral extrabranchial (VEB)
covers its respective ceratobranchial, except for ceratobranchial
5. The ventral portion of the pseudohyoid also has a corresponding ventral extrahyal element (VEH) (Fig. 12). Posterior
to Meckel‘s cartilage is the basihyal cartilage (BH), the ends of
which are fused to the first hypobranchials (HYB1). Medially
there are three hypobranchial cartilages and a large basibranchial cartilage (BB) (or basibranchial copula, which is fused
to hypobranchial 2 cartilages, HYB2). The basibranchial copula
is dorsoventrally flattened, broad, and projects posteriorly as a
ZOOLOGIA 28 (1): 97–111, February, 2011
slender extension. The second hypobranchial element has two
curved anterior extensions that almost reach the bashyal arch.
Immediately lateral to the second hypobranchial is the third
hypobranchial cartilage (HYB3), which is somewhat asymmetrical in relation to its antimere, and positioned at the same level
of ceratobranchials 2 and 3. The fourth hypobranchial (HYB4)
is circular and located in between hypobranchial 3, ceratobranchials 4 and 5, and the base of hypobranchial 2 (Fig. 12).
Scapulocoracoid. The pectoral girdle is rectangular, limited anteriorly by a rounded procondyle (PR) and posteriorly
by the more elongated metacondyle (MT). Between the
procondyle and metacondyle there is a truncated and elongated mesocondyle (MS) (Fig. 13). The distance between the
procondyle and mesocondyle is smaller than the distance between the mesocondyle and metacondyle. In the dorsal region
there is a small but clearly visible scapular process (SCP). There
are 17 small protuberances along almost all of the ventral extension of the girdle, below the condyles. The rear corner (RC)
is well developed. Two large lateral fenestrae are present. The
anterior fenestra (AFE) is between the mesocondyle and
procondyle. It has a more circular shape and is slightly wider
than the posterior fenestra. The posterior fenestra is subdivided
into dorsal and ventral fenestra, separated by a long, narrow
neopterygial process (NP). The posterior dorsal fenestra (PDF)
is oval and about the same size as the anterior fenestra (Tab.
V). The posterior ventral fenestra (PVF) is more elliptical, dorsoventrally flattened, and is about one-fourth the height of the
posterior dorsal fenestra.
Puboischiadic bar. The pelvic girdle or pubschiadic bar (Figs
14 and 15) is dorsoventrally flattened, transversely oriented, and
has three to four laterally situated iliac foramina (IF). The
prepelvic processes (PRP) are triangular and lateroanteriorly po-
Figure 13. Lateral view of scapuloracoid of D. mennii (UERJ 1008).
(AFE), anterior fenestra, (MS) mesocondyle, (MT) metacondyle,
(NP) neopterygial process, (PDF) posterior dorsal fenestra, (PR)
procondyles, (PVF) posterior ventral fenestra, (RC) rear corner,
(SCP) scapular process. Scale bar: 20 mm.
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
PRP
105
PTB
IF
IE
IP
14
15
Figures 14-15. Puboischiadic bar of D. mennii: (14) dorsal view of male (UERJ 2103); (15) ventral view of female (UERJ 2105). (PRP) prepelvic
processes, (PTB) transverse pelvic bar, (IE) iliac extension, (IF) iliac foramen, (IP) iliac process. Scale bars: 14 = 40 mm, 15 = 50 mm.
Table V. Measurements (mm) of the scapulocoracoid taken from
one specimen of D. mennii. Percentages are in relation to
scapulocoracoid total length; specimen is from the UERJ collection.
Measurements
Total length
Specimen 1008 (male)
mm
%
113
100.00
Maximum height
66
58.40
Premesocondyle length
72
63.70
Postmesocondyle length
45
39.80
Anterior fenestra maximum height
33
29.20
Anterior fenetra maximum length
31
27.40
Posterior dorsal fenestra height
24
21.20
Posterior dorsal fenestra length
30
26.50
Posterior ventral fenestra height
7
6.10
Posterior ventral fenestra length
25
22.12
sitioned. The well developed iliac process (IP) has a rounded
extremity and extends posteriorly from the iliac region. The
rounded, laterally situated iliac extension (IE) is smaller than
the iliac process. There is a sexual dimorphism in the posterior
part of the puboischiadic transverse bar (PTB), which is slightly
less arched and relatively smaller in males (Fig. 14) than in females (Fig. 15).
Clasper. The mixopterigial (clasper) skeleton consists of
three groups of cartilages: the basal, axial, and distal groups.
The basal group (not described here for D. menni because they
were lost in preparation) is formed by the b1, b2 (intermediate
proximal segments), and β cartilages. The axial group is represented by three fused cartilages: the axial (AX), dorsal marginal (DM), and ventral marginal (VM). The cartilages of the
distal group are the dorsal terminals (DT1, DT2 and DT3), ventral terminal (VT), and accessory terminals (ACT1 and ACT2)
(Figs 16 and 17).
Figures 16-17. Clasper skeleton of D. mennii (UERJ 2103), in dorsal
(16) and ventral (17) views. (ACT1) accessory terminal 1, (ACT2)
accessory terminal 2, (AX) axial, (DM) dorsal marginal, (DT1) dorsal
terminal 1, (DT2) dorsal terminal 2, (DT3) dorsal terminal 3, (VM)
ventral maginal, (VT) ventral terminal. Scale bars: 16-17 = 20 mm.
ZOOLOGIA 28 (1): 97–111, February, 2011
106
R. A. Moreira et al.
The axial cartilage extends throughout the entire length
of the mixopterigium. Its distal end is subdivided and less calcified; the medial segment suffers a slight torsion. Externally
the spermatic groove is located between the dorsal and ventral
marginal cartilages. The dorsal marginal cartilage (Fig. 16) extends from its articulation with the b2 and β cartilages (not
shown in Fig. 16) to the clasper glans region, anterior to the
terminal cartilages. The ventral marginal cartilage has a rounded
and expanded posterior end, and is broader than the dorsal
marginal cartilage (Figs 16, 17 and 26).
The distal region of the glans presents dorsal and ventral
components. The dorsal component is formed by three dorsal
terminal cartilages. The dorsal terminal 1 cartilage is long and
lacks the proximal shelf for the clasper dilator muscle. It is
subtriagular, slightly dorsal to the dorsal terminal 2 cartilage
and supported by almost the entire distal portion of the axial
cartilage. The proximal region of the dorsal terminal 1 cartilage is broad, with a rounded margin, and becomes more slender distally where it is twisted and covers the distal axial region (Figs 16, 17, 20 and 21). The dorsal terminal 2 cartilage is
subrectangular (Figs 16, 26 and 27), located between the dorsal
terminal 1 and the distal extension of the dorsal marginal cartilage. At the distal end of the dorsal terminal 2 cartilage is the
poorly calcified and short terminal bridge (TB), which reaches
the dorsal terminal 3 cartilage and the distal portion of the
axial cartilage (Figs 26 and 27). The dorsal terminal 3 extends
distally from the dorsal terminal 2 and fuses with the axial
cartilage at its less calcified portion (Figs 26 and 27).
The ventral component of the mixopterigium has the same
number of components as those of the dorsal component: one
ventral terminal and two acessory terminal cartilages (1 and 2).
The ventral terminal cartilage (Figs 16, 17, 18 and 19) is J-shaped,
with a pointed projection anteroventrally (Figs 17 and 19, see
arrow) which extends about 1/5 of the total length of the cartilage. The ventral and anterior aspects of the ventral terminal
cartilage support the anterior segment of the acessory terminal
1, located at the external clasper margin (Fig. 17). The accessory
terminal 1 is Y-shaped (Figs 17, 24 and 25). The most elongated
(anterior) branch is turned toward the outer clasper margin (Figs
16 and 17). A rod-shaped accessory terminal 2 cartilage is present
articulating with the distal end of the ventral marginal cartilage; its distal end also presents a slight torsion (Figs 17, 22 and
23). This cartilage is located at almost the limit of the dorsal and
ventral lobes of the mixopterigium, where it is slightly supported
by the dorsal terminal 1 and accessory terminal 1 cartilages.
DISCUSSION
Our morphological investigation of D. mennii revealed
additional characters that allow it to be distinguished from D.
trachyderma (summarized in Table VI). According to LEIBLE &
STEHMANN (1987), D. trachyderma is characterized by a rough
dorsal and ventral surface, covered with small denticles, but
ZOOLOGIA 28 (1): 97–111, February, 2011
lacks nuchal and mediodorsal thorns. As D. mennii has a relatively rough interbranchial region, and the rostral and interorbital regions also have coarse denticles, mistakes in the identification of both species have occurred (e.g. GOMES & PICADO
2001). Dipturus mennii, however, is unequivocally characterized by a continuous row of thorns from the nuchal region to
the first dorsal fin (we therefore confirm the observations of
GOMES & PARAGÓ 2001), and is much less course throughout.
Below we discuss further morphological features that separate
D. mennii from D. trachyderma and compare them to the morphology of other Dipturus species. Pelvic girdle morphology,
however, is not useful to distinguish D. mennii from D.
trachyderma. Comparisons of gill arches and synarcual cartilage were not possible due to lack of comparative data for D.
trachyderma and other Dipturus species.
Neurocranium
The neurocranium of D. mennii and D. trachyderma are
generally similar in proportions and in most structures. However, the neurocranium of D. mennii presents a unique ophthalmic process which overlies the ophthalmic foramen. In D.
trachyderma, the ophthalmic process is missing (L EIBLE &
STEHMANN 1987). The optic foramen in D. mennii is circular compared to the elongated optic foramen of D. trachyderma, but
this feature needs to be compared in more specimens of the
latter species before it can be employed to distinguish it from
D. mennii.
In both D. trachyderma and D. mennii there is a small
narrow groove in front of the anterior fontanelle which is identified by STEHMANN (1970) and HULLEY (1972) as a defining generic character, being considered by ISHIHARA & ISHIYAMA (1986)
the only really useful character to distinguish Dipturus from
the closely related Okamejei, which does not have this feature.
This narrow groove is also not found in Zearaja, the possible
sister-group of Dipturus (LAST & G LEDHILL 2007). As the rostral
groove is not present in other rajid taxa, its presence in Dipturus
may be derived. However, JEONG & N AKABO (2008) described
Dipturus wuhanlingi based on a juvenile specimen which does
not have the rostral groove. And previously, SÉRET (1989) had
described adults of Dipturus crosnieri as lacking the rostral groove
and, according to that author, this species exhibits other putative characters of Dipturus in accordance with the key for
Dipturus and Okamejei presented by ISHIHARA (1987). The lack of
the rostral groove anterior to the rostral cartilage can be a further derived character for these species, or perhaps they are
basal to other species of Dipturus; in any case they do not deny
the rostral groove as a diagnostic feature of Dipturus.
A long and stout rostrum is considered by MCEACHRAN &
MIYAKE (1990b) and MCEACHRAN & DUNN (1998) as plesiomorphic
within Rajidae. STEHMANN (1970), nonetheless, had emphasized
the importance of rostrum length in Dipturus taxonomy. CHEN
& JOUNG (1989) quantified rostral length for Dipturus as 60% of
the total length of neurocranium, setting it apart from Okamejei
in which rostral length is clearly less than 60%. Due to the
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
20
18
22
107
21
19
23
24
25
26
27
Figures 18-27. Dipturus mennii (UERJ 2103). (18-19) Ventral terminal cartilage: (18) in dorsal view; (19) ventral view. (20-21) Dorsal
terminal 1 cartilage: (20) in dorsal view; (21) ventral view. (22-23) Accessory terminal 2 cartilage: (22) in dorsal view; (23) ventral view.
(24-25) Accessory terminal 1 cartilage: (24) dorsal view; (25) ventral view. (26-27) Clasper skeleton: (26) ventral; (27) dorsal view, with
accessory terminal 1, accessory terminal 2, dorsal terminal 1, and ventral terminal cartilages removed. (DM) Dorsal marginal, (DT2)
dorsal terminal 2, (DT3) dorsal terminal 3, (TB) terminal bridge, (VM) ventral marginal. Scale bars: 18-21, 24-25 = 10 mm, 22-23 = 1 mm,
26-27 = 20 mm.
relation rostrum/total length of neurocranium, JEONG & NAKABO
(2008) identified their new species D. wuhanlingi as belonging
to Dipturus. Dipturus crosnieri also presents this relation (see
table 3 of SÉRET 1989), and so do D. mennii and D. trachyderma.
These proportions were also observed by HULLEY (1972) in all
species of Dipturus from South Africa, except D. pullopunctata
(rostrum some 57% of neurocranium length). In conclusion,
rostral proportions may also be derived for Dipturus.
Pectoral girdle
The pectoral girdle in Rajidae presents basically the same
rectangular shape (MCEACHRAN & COMPAGNO 1979, 1982). LEIBLE
& S TEHMANN (1987) described the pectoral girdle of D.
trachyderma showing two posterior ventral fenestrae, whereas
D. mennii has only one. The presence of two posterior ventral
fenestrae seems to be a specific character, as ISHIHARA & ISHIYAMA
(1986) show the pectoral girdle of seven species of Dipturus
ZOOLOGIA 28 (1): 97–111, February, 2011
108
R. A. Moreira et al.
Table VI. Summary of some relevant morphological characters which may distinguish D. menni from D. trachyderma..
Characters
D. mennii
D. trachyderma
Nuchal thorns
5-7
Absent
Mediodorsal row
18-25
Absent
Lateral tail thorns
6-26
4-30
Interdorsal thorns
1-3
0-4
Ophthalmic foramen
Ventrally open groove, associated to ophthalmic
process
Fully enclosed, without ophthalmic process
Anterior scapulocoracoid fenestra
Circular
Laterally elongated
Posterior ventral fenestra of
scapulocoracoid
One fenestra
Two fenestrae
Acessory terminal 1
Anterior segment with regular, smooth surface
Anterior segment with irregular surface
Acessory terminal 1
Largest segment contacts the ventral terminal
cartilage
Largest segment does not contact the
ventral terminal cartilage
Ventral terminal
Anterior and ventral tip short, about the 1/5
length of component
Anterior and ventral tip long, about the 1/3
length of component
Dorsal terminal 2
Anterior margin posterior to dorsal terminal 2
Anterior margin anterior to dorsal terminal 2
Accessory terminal 2
Not elongated, twisted at posterior tip of
accesory terminal 2
Elongated, only slightly twisted at posterior
tip of acessory terminal 2
Terminal bridge
Short, arising between the dorsal terminal 2 and Elongated, wedged between dorsal terminal
dorsal teriminal 3
1 and dorsal terminal 2
from North Pacific, all presenting just one ventral fenestra. The
shape and size of the anterior and posterior fenestrae can also
vary greatly according to species. The anterior fenestra of D.
trachyderma, according to LEIBLE & STEHMANN (1987), suffers a
constriction due to the elongation of the procondyle and
mesocondyle, unlike in D. mennii in which the anterior fenestra is quite circular.
Claspers
Dipturus mennii and D. trachyderma have subtle, but reliable differences in clasper skeleton. LEIBLE & STEHMANN (1987)
gave a detailed description of the external and internal structures of the mixopterigium of D. trachyderma. In D. trachyderma
these authors showed that the anterior segment of the accessory terminal 1 cartilage has an irregular surface, different from
D. mennii in which it is entirely smooth. In D. mennii the largest segment of the accessory terminal 1 contacts the ventral
terminal cartilage, a condition also seen in D. trachyderma, D.
batis, and D. oxyrinchus, as demonstrated by LEIBLE & STEHMANN
(1987) and STEHMANN (1970). ISHIYAMA (1958) showed that the
same condition occurs in Japanese Dipturus species. HULLEY
(1972), however, found that in the South African Dipturus doutrei
and D. lanceorostrata the ventral terminal cartilage does not
firmly articulate with the accessory terminal 1.
In D. trachyderma, the ventral terminal cartilage is situated more anteriorly (LEIBLE & S TEHMANN 1987), contacting the
ventral marginal to a greater extent than in D. mennii, in which
the ventral terminal is more posteriorly positioned and so con-
ZOOLOGIA 28 (1): 97–111, February, 2011
tacts the accessory terminal 1 cartilage more than it does the
ventral marginal cartilage. The ventral terminal cartilage of D.
mennii presents an anteroventral and sharp segment (Fig. 19,
see arrow) that is about 1/5 of the total length of the component. In D. trachyderma, this segment is greater, achieving about
1/3 of the length of the ventral terminal (as inferred from LEIBLE
& S TEHMANN 1987). Furthermore, the posterior portion of the
ventral terminal is much more spatulate in D. trachyderma than
in D. mennii.
According to LEIBLE & STEHMANN (1987), the accessory terminal 2 cartilage in D. trachyderma is elongated, rod-shaped,
and slightly twisted, with a flattened distal end, but exactly
where this torsion takes place is not so clear. The torsion in D.
mennii occurs only at the posterior tip of the accessory terminal 2 cartilage (Figs 22 and 23), but not as much as in Dipturus
crosnieri, in which this cartilage is highly twisted distally, appearing J-shaped (SÉRET 1989). This cartilage can also present a
well developed and posteriorly pointed process in some Japanese Dipturus (e.g. D. macrocauda and D. gigas), Okamejei (e.g.
O. hollandi and O. kenojei), according to ISHIYAMA (1958), and D.
pullopunctata (HULLEY 1972). The accessory terminal 2 cartilage
therefore varies significantly among species and may have great
importance in Dipturus taxonomy.
The dorsal terminal 1 cartilage is somewhat similar in D.
trachyderma and D. mennii, but in the former species it reaches
farther anteriorly (beyond the level of the dorsal terminal 2,
whereas in D. mennii its anterior margin is posterior to dorsal
Morphological description of Dipturus mennii and its differentiation from Dipturus trachyderma
terminal 2), and is relatively wider posteriorly. According to
LEIBLE & STEHMANN (1987) the shape of this cartilage is very similar
in all representatives of Dipturus, including the lack of the proximal support (or proximal edge) for the insertion of the dilator
muscle, as was also confirmed by H ULLEY (1972) for D.
pullopunctata, D. lanceostrata, and D. doutrei.
The dorsal terminal 2 cartilage is more slender in D.
trachyderma in comparison to the dorsal terminal 2 of D. menni.
According to HULLEY (1972), in the South African D. doutrei and
D. pullopunctata, a short, cartilaginous bridge (the terminal bridge)
is well-developed, connecting the dorsal terminal 2 to the axial
cartilage. In D. mennii the terminal bridge is short and arises
between the dorsal terminal 2 and dorsal terminal 3, attaching
both cartilages to the axial cartilage, whereas in D. trachyderma
the terminal bridge is much more elongated and wedged in between dorsal terminals 1 and 2 (LEIBLE & STEHMANN 1987).
In conclusion, Dipturus mennii and D. trachyderma are
clearly distinct species. The main diagnostic characters that
separate them are found in squamation patterns (nuchal and
mediodorsal thorns, number of thorns on lateral tail),
neurocranial features (ophthalmic foramen, ophthalmic process), anterior and posterior ventral fenestra of scapulocoracoid,
and mixopterigial skeleton (accessory terminals 1 and 2, terminal bridge, ventral terminal, dorsal terminals 1 and 2). However, there is a significant gap in our knowledge concerning
the synarcual cartilage and gill arches among species of Dipturus,
and therefore descriptive studies of these elements are needed
in addition to those typically done on the neurocranium and
clasper. Furthermore, a general revision of the diagnostic characters of Dipturus and its included species are necessary in light
of the morphological similarities with the putatively closely
related genera Okamejei and Zearaja; however, the anterior rostral groove, elevated rostral proportions, and specific configuration of the ventral terminal cartilage may indeed be derived
characters for Dipturus.
ACKNOWLEDGEMENTS
We thank C.M. da Cunha and C.M. Vooren for the donation of specimens used in this study, and H.R.S. Santos for suggestions and discussion. The program PROCIÊNCIA/FAPERJ is
acknowledged for grants awarded to the second author. The
third author is supported by research fellowships from CNPq
(303061/2008-1) and Fapesp (2010/51193-5).
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Submitted: 01.XII.2009; Accepted: 26.IX.2010.
Editorial responsibility: Wolmar B. Wosiacki
ZOOLOGIA 28 (1): 97–111, February, 2011