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Phylogenetic inferences on the systematics of squaliform sharks based on

elasmobranch scapular morphology (Chondrichthyes: Elasmobranchii)

Article  in  Zoological Journal of the Linnean Society · March 2018

DOI: 10.1093/zoolinnean/zlx051

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 Zoological Journal of the Linnean Society, 2017, XX, 1–17. With 19 figures.

Phylogenetic inferences on the systematics of squaliform

sharks based on elasmobranch scapular morphology
(Chondrichthyes: Elasmobranchii)
JOÃO PAULO C. B. DA SILVA1*, DIEGO F. B. VAZ2 and MARCELO R. DE CARVALHO1
1
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Trav. 14,
no. 101, 05508-090, São Paulo, SP, Brazil
2
Virginia Institute of Marine Science, College of William and Mary, Rt. 1208, 1375 Greate Road,
Gloucester Point, VA 23062, USA

Received 8 December 2016; revised 3 May 2017; accepted for publication 29 June 2017

The scapulae of elasmobranchs project dorsolaterally from their fusion with the coracoid bar of the pectoral gir-
dle, serving as anchoring points for the cucullaris, trunk and appendicular muscles and as articular points for the
pectoral-fin skeleton. The scapulae of many elasmobranch taxa are described, with an emphasis on variations in the
posterior margin, in an effort to reveal characters of phylogenetic relevance. In particular, phylogenetic information
from the scapula was found for some squaliform sharks. Representatives of Dalatiidae, Somniosidae, Oxynotidae
and Etmopteridae have a process on the ventral third of the posterior margin of the scapula, providing an additional
surface for anchoring the origin of the appendicular muscle: the levator pectoralis. The ventral scapular process in
Dalatiidae, Somniosus and Etmopterus is remarkably developed. This contrasts with an absent or weakly devel-
oped ventral triangular process observed in remaining squaliforms and other shark taxa. A single dorsal projec-
tion of the scapulae is restricted for Carcharhinidae and Centrophorus and provides an additional anchoring point
for the m. epaxialis. Most representatives of Somniosidae (except Somniosus), Trigonognathus and some genera of
Scyliorhinidae, Proscylliidae and Triakidae have both dorsal and ventral triangular processes. These structures are
described and discussed in the context of previous morphological and molecular phylogenies of elasmobranchs.

ADDITIONAL KEYWORDS:  elasmobranchs – galeomorphs – m. levator pectoralis – scapula – morphology –

squalomorphs.

INTRODUCTION Silva, Vaz & Carvalho, 2015). The pectoral girdle is

fundamental to the biomechanics and locomotion of
The pectoral girdle of elasmobranch fishes is composed
elasmobranchs (e.g. Wilga & Lauder, 2001, 2004; Maia,
of a transverse, rod-like coracoid that is laterally fused
Wilga & Lauder, 2012). The pectoral girdle is inde-
to the perpendicular scapular cartilages, forming a
pendent of the vertebral column in sharks, but in rays,
‘U’-shaped structure (Daniel, 1934; Compagno, 1973,
the dorsal suprascapulae are tightly bonded to the
1977; Cappetta, 2012; Silva & Carvalho, 2015). The
synarcual cartilage, a derived condition for the group
girdle provides anchorage for epaxialis and hypaxi-
related to increased support for the disc allowing
alis trunk musculature on its posterolateral surface,
their particular pectoral fin-based mode of locomotion
for the branchiomeric cucullaris muscle on its antero-
(Compagno, 1973; Wilga & Lauder, 2004; Rosenberger,
dorsal surface, the hypobranchial musculature on its
2001).
anteromedial surface, and the levator and depressor
The articular region of the pectoral basals varies
pectoral muscles on its posteroventral surface (Daniel,
significantly among elasmobranchs, with different
1934; Liem & Summers, 1999; Goto, Nishida & Nakaya,
arrangements of facets and condyles (or both), and is
1999; Gudo & Homberger, 2002; Tomita et al., 2014;
an important source of information for systematic and
phylogenetic studies of lower and higher elasmobranch
*Corresponding author. E-mail: jpcbs@ib.usp.br taxa (e.g. McEachran & Compagno, 1979, 1982; Shirai,

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 2  J. P. C. B. DA SILVA ET AL.
1992a, b, 1996; Carvalho, 1996; McEachran & Dunn,
1998; Silva & Carvalho, 2015). The scapulae, however,
also vary considerably among elasmobranch taxa; they
range from long and stout, short and stout, to long and
distally narrow, culminating in scapular processes
that are nearly filiform in some groups (Silva, 2014;
Silva & Carvalho, 2015). The anterior and posterior
surfaces of the scapulae are also highly variable, with
nearly straight, concave, convex or sigmoidal outlines.
This study reports the morphological variation in
the posterior scapular surface of elasmobranchs and
its arrangement with the pectoral musculature. This
surface can be nearly straight to sinuous and bears
one or two distinct and posteriorly projected processes.
These morphological variations, as well as their sys-
tematic implications, are discussed in the context of
previous morphological and molecular hypotheses of
elasmobranch intrarelationships.
MATERIAL AND METHODS
The representatives of elasmobranch taxa were mostly
manually dissected. All musculature covering the
pectoral girdle was removed to expose the skeleton.
Cleared and stained material was prepared following
Dingerkus & Uhler (1977). Terminology for skeletal
structures mostly follows Daniel (1934), Shirai (1992b),
Compagno (1999) and Silva & Carvalho (2015). The
abbreviation total length (TL) refers to total length. The
cladograms were built with the software MESQUITE
version 3.11 (Maddison & Maddison, 2016). Character
optimizations were carried out using the parsimony
and unordered characters options in MESQUITE.
Material examined was from the following institu-
tions: American Museum of Natural History, New York
(AMNH); Bernice Pauahi Bishop Museum, Honolulu,
Hawaii (BPBM); California Academy of Sciences, San
Francisco (CAS); Florida Museum of Natural History,
Gainesville (FLMNH); Hokkaido University Museum,
Hakodate (HUMZ); Museu Nacional, Rio de Janeiro
(MNRJ); Muséum national d’Histoire naturelle, Paris
(MNHN); Natural History Museum, London (BMNH);
National Museum of Marine Biology and Aquarium,
Pingtung, Taiwan (NMMBP); National Museum of
Nature and Science, Tsukuba, Japan (NSMT); Museu
de Zoologia da Universidade de São Paulo, São Paulo
(MZUSP); National Museum of Natural History,
Smithsonian Institution, Washington, DC (USNM);
Universidade do Estado do Rio de Janeiro, Rio de
Janeiro (UERJ).
Anatomical abbreviations are as follows: adf, anter-
odorsal fenestra; avf, anteroventral fenestra; cc, cuc-
ullaris; cor, coracoid bar; df, diazonal foramen; dp1,
depressor pectoralis 1; ep, epaxialis; hp, hypaxialis;
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idt, indentation; lp, levator pectoralis; msc, mesocon-
dyle; mtc, metacondyle; p, propterygium; par, pectoral
articular region; pdf, posterodorsal fenestra; pc, pro-
condyle; pcr, posterior corner; pdt, posterodorsal trian-
gular process of scapula; pvf, posteroventral fenestra;
pvt, posteroventral triangular process of scapula; scl,
scapula; scp, scapular process; ssc, suprascapula.
Material analysed
Heterodontidae: Heterodontus zebra: MZUSP
uncat. (male, 305-mm TL). Ginglymostomatidae:
Ginglymostoma cirratum: CAS 232210 (male, 485-
mm TL). Stegostomatidae: Stegostoma fasciatum:
CAS 80843 (female, 350-mm TL). Mitsukurinidae:
Mitsukurina owstoni: MZUSP uncat. (female, 1112-
mm TL). Pseudocarchariidae: Pseudocarcharias
kamoharai: MZUSP 112028 (female, 910-mm TL).
Alopiidae: Alopias superciliosus: UERJ 735.2 (male,
545-mm TL). Lamnidae: Lamna nasus: USNM
201731 (female, 750-mm TL); Isurus oxyrinchus:
USNM 201733 (female, 745-mm TL). Proscylliidae:
Eridacnis radcliffei: CAS 34861 (female, 230-mm
TL). Scyliorhinidae: Apristurus parvipinnis: UERJ
uncat. (male, 588-mm TL); Parmaturus xaniurus:
CAS 37513 (female, 410-mm TL); Scyliorhinus haeck-
elii: MZUSP 112024 (male, 385-mm TL). Triakidae:
Mustelus griseus: MZUSP uncat. (male, 280-mm TL).
Hemigaleidae: Hemigaleus microstoma: HUMZ 01823
(male, 850-mm TL). Carcharhinidae: Rhizoprionodon
lalandii: MZUSP uncat. (female, 420-mm TL);
Carcharhinus porosus: CAS 56629 (female, 550-mm
TL); Galeocerdo cuvier: MZUSP 112027 (female, 895-
mm TL); Prionace glauca: UERJ 1866 (male, 453-mm
TL); Triaenodon obesus: CAS su14498 (female, 490-
mm TL); Scoliodon laticaudus: CAS 31381 (male,
525-mm TL). Sphyrnidae: Sphyrna zygaena: CAS
56507 (male, 435-mm TL). Chlamydoselachidae:
Chlamydoselachus anguineus: MZUSP 110974 (male,
1345-mm TL). Hexanchidae: Heptranchias perlo:
MZUSP 110475 (male, 821-mm TL); Hexanchus griseus:
CAS uncat. (male, 1300-mm TL). Echinorhinidae:
Echinorhinus cookei: MZUSP uncat. (female, 1500-
mm TL); Echinorhinus brucus: FLMNH 103000 (male,
300-mm TL). Etmopteridae: Centroscyllium fabricii:
USNM 35579 (female, 530-mm TL); FLMNH 159844
(female, 420-mm TL); Etmopterus bigelowi: MNRJ
30217 (female, 570-mm TL); UERJ 2172.3 (male, 470-
mm TL); Etmopterus pusillus: USNM 221042 (female,
530-mm TL); Trigonognathus kabeyai: MZUSP uncat.
(male, 366-mm TL). Somniosidae: Centroscymnus
coelolepis: MNRJ 30224 (female, 580.5-mm TL);
USNM 38079 (female, 450-mm TL); Centroscymnus
owstonii: FLMNH 27957 (male, 311-mm TL);
UERJ A.1460 (female, 950-mm TL); Centroselachus
 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  3

crepidater: AMNH 55521 (male, cleared and stained);

AMNH 58099 (female, 299-mm TL); Scymnodalatias
albicauda: HUMZ 129360 (male, 171-mm TL);
Scymnodon ichiharai: NMMBP 15843 (female, 1317-
mm TL); Scymnodon ringens: BMNH 1991.7.9.686-690
(female, 507-mm TL); Somniosus rostratus: BMNH
1906.11.12.7 (juvenile, unknown sex, skeleton only,
~500-mm TL); MZUSP uncat. (male, 1319-mm TL);
Zameus squamulosus: HUMZ 143441 (female, 579-mm
TL); USNM 94520 (female, 351-mm TL). Oxynotidae:
Oxynotus bruniensis: USNM 320641 (female, 465-mm
TL); HUMZ 91383 (male, 545-mm TL). Dalatiidae:
Dalatias licha: USNM 157844 (female, 361-mm TL);
MZUSP uncat. (female, 464-mm TL); Euprotomicrus
bispinatus: BPBM 40404 (female, 255-mm TL); Isistius
brasiliensis: MNHN 1996-0465 (male, 409-mm TL);
Squaliolus laticaudus: AMNH 15731 (female, 361-
mm TL). Centrophoridae: Centrophorus granulosus:
USNM 220221 (female, 395-mm TL); Deania calcea:
USNM 203495 (female, 700-mm TL); MZUSP uncat.
(female, 1004-mm TL). Squalidae: Squalus acanthias:
HUMZ 30291 (male, 575-mm TL); Squalus megalops:
MZUSP 110973 (female, 512-mm TL). Squatinidae:
Squatina guggenheim: MZUSP 110871 (female, 450-
mm TL). Pristiophoridae: Pristiophorus japonicus:
MZUSP uncat. (male, 510-mm TL). Rajidae: Dipturus Figure 1.  Schematic delimitation of the scapula in a
mennii: UERJ 2104 (female, pectoral girdle only); shark (A) and a ray (B, C) defining the boundaries of these
Gurgesiella atlantica: MZUSP uncat. [female, 210-mm parts. Lateral (A, B) and dorsal (C) views of the scapula.
disc width (DW)]. Arhynchobatidae: Atlantoraja A, Squalus megalops (MZUSP 110973, female, 512-mm
cyclophora: MZUSP uncat. (male, 364-mm DW). TL). B, C, Rhynchobatus djiddensis (CAS uncat., female,
Rhynchobatidae: Rhynchobatus djiddensis: CAS 500-mm TL). In (A, B) anterior to left, dorsal to top; in (C),
uncat. (female, 500-mm TL). anterior to left.

on the developmental stage (Fig. 1A). The bound-

RESULTS
The scapulae (scl) correspond to the dorsal projec-
tions of the pectoral girdle, lateral to the transverse
and ventral coracoid bar (cor) (Fig. 1). They are a
variable outline among elasmobranch taxa and
usually end in distal scapular processes (scp) that
may be well developed or discrete. The anterior and
posterior surfaces of the scapula vary considerably:
straight, concave, convex or both. The posterior sur-
face of the scapulae has a fossa (idt) for the attach-
ment of the pectoral levator muscle (lp), which in
some taxa contains a posteriorly directed process
(pvt) that provides an additional anchoring point
for this muscle (Fig. 2). The scapular process is con-
tinuous and dorsal to the scapula; some shark taxa
may have a posteriorly directed process at its base
(pdt). The scapular process is short in sharks (about
one third of scapular length), and detached from
the scapula in some taxa (e.g. Squalus), depending
ary between the scapula and the scapular process is
demarcated by a faint and distal transverse ridge in
many taxa, indicating where these structures become
fused during development. However, in many shark
taxa (especially galeomorphs) this distal transverse
ridge is not evident.
In rays, the extension of the scapular process varies
considerably. The scapula, defined as the lateral aspect of
the scapulocoracoid, with the pectoral fenestrae and con-
dyles (Fig. 1B). The scapular process starts just dorsal to
the dorsal fenestra and projects dorsomedially in rela-
tion to the body axis (Fig. 1C). The scapular processes are
narrower compared to the scapulae and are associated
with the suprascapulae (ssc). They also vary consider-
ably in extension among orders of Batoidea, short in the
Rajiformes but usually long in the Rhinopristiformes,
Torpediniformes and Myliobatiformes (except for mem-
bers of the families Gymnuridae and Myliobatidae).
Different conditions of the posterior margin of the scap-
ular process are described below.

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 4  J. P. C. B. DA SILVA ET AL.
Figure 2.  Left lateral view of the scapula of Somniosus
rostratus (MZUSP uncat., male, 1319-mm TL) depicting its
associated pectoral musculature. Anterior to left, dorsal to
top.
Posterior margin of the scapula (scl) with a
ventral indentation and lacking a posterior
process (pdt and/or pvt)
(coded in white in Figs 18, 19)
This condition was observed in most elasmobranch
taxa (Figs 3–9). The posterior margin of the scapula
(scl) is smooth and lacks any sort of process on its sur-
face. The posterior surface of the scapula varies from
straight to sinuous; when sinuous, the posterior mar-
gin can be either concave, convex or a combination of
both. The ventral portion of the posterior margin of
the scapulae has an indentation (idt), varying from
faint (e.g. Heterodontiformes) (Fig. 3B) to prominent
(e.g. Lamnidae) (Fig. 4B). Although this indentation
is remarkable in some groups, it does not form a dis-
tinct posteriorly directed process (as observed in other
shark taxa; see below). The surface of this indentation
is slightly flattened and serves as an anchoring point
for the m. levator pectoralis.
In Heterodontiformes and Orectolobiformes (Fig. 3B,
C), the scapula is tall (slightly shorter than the cora-
coid bar), stout and has similar proportions through its
entire extension, except distally, where it tapers and
forms a rhomboidal scapular process (scp). Basally,
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the scapula is pierced by a small and nearly circular
diazonal foramen (df) and has a faint posterior inden-
tation, which is somewhat flattened and dorsal to the
pectoral-fin articulations. In Carcharhiniformes (Figs
5, 6), the scapula is also tall (about equal in length to
the coracoid bar), has a wide base and tapers dorsally
culminating occasionally in a nearly filiform scapular
process (e.g. Parmaturus, Apristurus) (Figs 5B, C). On
its ventral lateral edge, the scapula is pierced by an
enlarged and circular diazonal foramen (two diazonal
foramina are present in Triakidae and Hemigaleidae).
The proximal portion of the scapula, immediately dor-
sal to the articular region, also has a shallow indenta-
tion for the m. levator pectoralis (except members of
the Carcharhinidae and Scyliorhinidae that can have
one or two posterior processes, and are therefore inter-
preted as bearing different conditions; see below). The
scapular region of most lamniforms (Mitsukurinidae,
Pseudocarchariidae, Alopiidae) (Figs 3A, 4A, C) has a
similar pattern to that observed in Carcharhiniformes
(Figs 5, 6). However, the outline observed in Lamnidae
(Fig. 4B) is noticeably different. The scapula is consid-
erably shorter (approximately half of the length of the
scapula in Pseudocarcharias) and nearly rectangular,
tapering faintly towards its quadrangular scapular
process. There is also an indentation in the lower por-
tion of the scapulae anchoring the m. levator pectoralis
(lp). This condition is clear in L. nasus and I. oxyrin-
chus (Lamnidae) (Fig. 4B).
All representatives of Hexanchiformes (Figs 7A–C)
have a pattern that resembles most carcharhini-
forms, except for the reduced diazonal foramen.
The scapula is only enlarged basally and tapers
dorsally, culminating in a filiform and poorly calci-
fied scapular process (detached from the scapula in
C. anguineus). There is a posterior flattened area
immediately above the pectoral articulation anchor-
ing the m. levator pectoralis. In E. cookei (Fig. 8A),
the scapula is greatly enlarged at its base and tapers
distally, ending in a nearly rhomboid scapular pro-
cess. The posterior margin of the scapula is slightly
convex and lacks any process. However, a nearly oval,
flattened area in the ventral portion of the posterior
margin serves as an anchoring point for the m. leva-
tor pectoralis. Representatives of Squaliformes, such
as Deania (Centrophoridae) (Fig. 9A) and Dalatias
(Dalatiidae) (Fig. 8B), also have a continuous poste-
rior scapular surface, lacking any sort of posterior
processes. In these species, the scapula is basally
thick and tapers somewhat towards its tip, ending
in a broadly pointed scapular process. In Squatina
(Fig. 9B), the scapula is tall, stout and tapers
faintly from its base towards its tip, terminating
in a scapular process that varies from rectangular
to triangular. The anterior and posterior margins
 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  5

Figure 3.  Left lateral views of the scapulae of members of Galeomorphii. A, Mitsukurina owstoni (MZUSP uncat., female,
1112-mm TL). B, Heterodontus zebra (MZUSP uncat. male, 305-mm TL). C, Stegostoma fasciatum (CAS 80843, female, 350-
mm TL). Anterior to left, dorsal to top.

Figure 4.  Left lateral views of the scapulae of members of Galeomorphii. A, Pseudocarcharias kamoharai (MZUSP 112028,
female, 910-mm TL). B, Lamna nasus (USNM 201731, female, 750-mm TL). C, Alopias superciliosus (UERJ 735.2, male,
545-mm TL). Anterior to left, dorsal to top.

Figure 5.  Left lateral views of the scapulae of members of Galeomorphii. A, Hemigaleus microstoma (HUMZ 01823, male,
850-mm TL). B, Parmaturus xaniurus (CAS 37513, female, 410-mm TL). C, Apristurus parvipinnis (UERJ uncat., male, 588-
mm TL). Anterior to left, dorsal to top.

of the scapula are also nearly straight, resembling compressed area on the posterior margin, just above
Heterodontiformes and Orectolobiformes (Figs 3B, the pectoral articulation for attaching the m. levator
C). There is also a flattened or anteroposteriorly pectoralis. In Pristiophorus (Fig. 9C), the scapula is

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 6  J. P. C. B. DA SILVA ET AL.

Figure 6.  Left lateral views of the scapulae of members of Galeomorphii. A, Triaenodon obesus (CAS su14498, female, 490-
mm TL). B, Sphyrna zygaena (CAS 56507, male, 435-mm TL). Anterior to left, dorsal to top.

Figure 7.  Left lateral views of the scapulae of members of Squalomorphii. A, Chlamydoselachus anguineus (MZUSP
110974, male, 1345-mm TL). B, Hexanchus griseus (CAS uncat., male, 1300-mm TL). C, Heptranchias perlo (MZUSP 110475,
male, 821-mm TL). Anterior to left, dorsal to top.

Figure 8.  Left lateral views of the scapulae of members of Squalomorphii. A, Echinorhinus cookei (MZUSP uncat., female,
1500-mm TL). B, Dalatias licha (USNM 157844, female, 361-mm TL). C, Squalus acanthias (HUMZ 30291, male, 575-mm
TL). Anterior to left, dorsal to top.

basally enlarged and tapers dorsally, ending in an and distally convex. The posterior margin also has a
acute scapular process. The anterior margin of the shallow concave indentation on its ventral third, dor-
scapula is basally convex and concave distally, con- sal to the pectoral articulation, where the m. levator
trary to its posterior margin which is basally concave pectoralis is anchored.

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 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  7

Posterodorsal process on scapula forming a G. atlantica (Rajidae) (Fig. 10A) and A. cyclophora

‘posterior corner’ (coded in red in Figs 18, 19)
In rays, the scapula is highly variable, but vis-
ibly anteroposteriorly expanded and dorsoventrally
short when compared to sharks. The extension of the
scapular process varies from short (one fourth of the
dorsoventral scapular length; e.g. Rajiformes) to tall
(equal to or greater than the dorsoventral scapular
length) in Torpediniformes, Rhinopristiformes and
some Myliobatiformes (e.g. Dasyatidae, Urolophidae,
Potamotrygonidae). The anterior and posterior sur-
faces of the scapula vary from faintly to strongly
convex and host the procondyle and metacondyle,
respectively. In D. mennii (Rajidae) (Fig. 10B),
(Arhynchobatidae) (Fig. 10C), a nearly triangular
posterior process is at the posterodorsal corner of the
scapula (‘rear corner’ of McEachran & Compagno,
1979, 1982; McEachran & Stehmann, 1984). This pos-
terior process (pcr) is posterodorsal to the pectoral
condyles and fenestrae (Fig. 10).
The homology of the posterior corner is uncer-
tain. It is topologically similar to the inferior process
observed in some shark taxa. However, due to its
restricted distribution (present only in rajiform fami-
lies), we are regarding the posterior process of skates
as non-homologous to the inferior process observed
in sharks.

Figure 9.  Left lateral views of the scapulae of members of Squalomorphii. A, Deania calcea (MZUSP uncat. female, 1004-
mm TL). B, Squatina guggenheim (MZUSP 110871, female, 450-mm TL). C, Pristiophorus japonicus (MZUSP uncat., male,
510-mm TL). Anterior to left, dorsal to top.

Figure 10.  Left lateral views of the scapulae of representatives of Rajiformes. A, Gurgesiella atlantica (MZUSP uncat.,
female, 210-mm DW). B, Dipturus mennii (UERJ 2104, female, DW not available). C, Atlantoraja cyclophora (MZUSP
uncat., male, 364-mm DW). Anterior to left, dorsal to top.

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 8  J. P. C. B. DA SILVA ET AL.

A single posterodorsal process (pdt) on the
dorsal third of the scapula or at the base of the
scapular process (coded in yellow in Figs 18, 19)
In this condition, the scapula is basally expanded and
tapered dorsally, terminating in an acute and eventu-
ally posteriorly curved scapular process (e.g. G. cuvier)
(Fig. 11B). Additionally, the anterior margin of the
scapula is concave and its posterior margin convex.
The base of the scapula has a wide circular diazonal
foramen anterior to the pectoral articular region.
Centrophorus granulosus (Centrophoridae) (Fig. 11A)
has a similar posterior process in the upper third of the
scapula at the base of the scapular process (although
there is no clear distinction between the scapular pro-
cess and scapula). However, the anterior margin of
C. granulosus has an additional symmetrical anterior
process on the anterior margin of the scapula that is
not as arched and does not taper distally as observed in
Carcharhinidae. The scapula of C. granulosus is wide
at its base and tapers toward the ventral origin of both
anterior and posterior processes. The scapular process
is basally wide (wider than the dorsal portion of the
scapula), forming a rhomboidal distal tip. The scapula
is nearly straight posteriorly, being convex only at the
level of the posterior process. A small diazonal foramen
pierces the base of the scapula just anterior to the pec-
toral condyle.
Most of the representatives of Carcharhinidae have
a filiform scapular process, with a rounded projec-
tion (pdt) on the base of the posterior margin (e.g.
Rhizoprionodon spp., P. glauca, G. cuvier, Carcharhinus
spp., S. laticaudus). The shape of this projection var-
ies from wide, shallow and rounded (Fig. 11B, C), to
pointed and nearly triangular (e.g. S. laticaudus)
(Fig. 12B). However, it may be absent in some repre-
sentatives of this family (e.g. T. obesus) (Fig. 6A).

Figure 11.  Left lateral views of the scapulae of a squaliform (A) and members of the Carcharhiniformes (B, C). A,
Centrophorus granulosus (USNM 220221, female, 395-mm TL). B, Galeocerdo cuvier (MZUSP 112027, female, 895-mm TL).
C, Prionace glauca (UERJ 1866, female, 453-mm TL). Anterior to left, dorsal to top.

Figure 12.  Left lateral views of the scapulae of members of the Carcharhiniformes. A, Carcharhinus porosus (CAS 56629,
female, 550-mm TL). B, Scoliodon laticaudus (CAS 31381, male, 525-mm TL). Anterior to left, dorsal to top.

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 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  9

Figure 13.  Left lateral views of the scapulae of members of Squaliformes. A, Centroscyllium fabricii (USNM 35579, female,
530-mm TL). B, Etmopterus pusillus (USNM 221042, female, 530-mm TL). C, Isistius brasiliensis (MNHN 1996-0465, male,
409-mm TL). Anterior to left, dorsal to top.

A single ventral triangular process (pvt) on

the posterior margin of the scapula (coded in
blue in Figs 18, 19)
In E. pusillus, C. fabricii, Squaliolus laticaudus,
Somniosus rostratus, I. brasiliensis and E. bispinatus,
the scapula is enlarged at its base and tapers gradu-
ally dorsally, culminating in a broadly pointed scapular
process (the same condition observed in most squali-
forms) (Figs 13, 14). The base of the scapula has a small
diazonal foramen, positioned anteriorly to the pectoral
articular region. The anterior margin of the scapula is
concave and has a faint, wide and shallow convex pro-
jection at its base. The posterior margin of the scapula Figure 14.  Left lateral views of the scapulae of members of
is slightly convex and has a prominent inferior trian- Squaliformes. A, Euprotomicrus bispinatus (BPBM 40404,
gular process at its ventral third (pvt). This process is female, 255-mm TL). B, Somniosus rostratus (MZUSP
posteriorly oriented and defines the dorsal limit where uncat., male, 1319-mm TL). Anterior to left, dorsal to top.
the m. levator pectoralis is attached to the scapula. The
attachment of this muscle extends from the tip of the some carcharhiniform representatives (Scyliorhinus,
triangular process to the ventral edge of the indenta- Mustelus and Eridacnis) also have a feeble inferior
tion immediately dorsal to the pectoral articulation. process, but with weakly developed dorsal triangular
In Centroscyllium (Fig. 13A), Isistius (Fig. 13C) and processes (Figs 15–17).
Euprotomicrus (Fig. 14A), this ventral process is not as
marked, as in the species mentioned above. The scapula
of Isistius and Euprotomicrus is proportionally shorter Two posterior triangular processes (pdt, pvt)
compared to other species and in Isistius, Euprotomicrus delimiting a posteromedian scapular concavity
and Squaliolus, the scapula also tapers dorsally to cul- (coded in black in Figs 18, 19)
minate in an acute and nearly filiform scapular process. In Z. squamulosus, Centroscymnus spp., Scymnodon
Isistius has a markedly arched scapula with a strongly spp., Scymnodalatias, Centroselachus, Proscymnodon
convex anterior margin and concave posterior margin. (Somniosidae), Oxynotus (Oxynotidae) and T. kabeyai
This prominent inferior triangular process on the (Etmopteridae) (Figs 15, 16), the base of the scapula is
posterior margin of the scapula was not found in expanded at its junction with the coracoid bar and has
any other member of the Squaliformes. Squalidae a small and rounded diazonal foramen. The scapula is
(Squalus spp.) (Fig. 8C) have only a faint inferior usually stout and tapers slightly dorsally, terminating
projection. Most somniosids, Trigonognathus and in a broadly pointed scapular process. In some cases

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 10  J. P. C. B. DA SILVA ET AL.

(Zameus, C. coelolepis, C. owstonii, Oxynotus, S. rin-
gens, S. ichiharai, Scyliorhinus spp.) (Figs 15–17), the
scapula presents a subtle anteroposterior compression
at its proximal half. The scapula is also oriented poste-
riorly to some extent and has a concave anterior mar-
gin and convex posterior margin. The anterior margin
of the scapula has a wide and shallow convex projection
at its medial portion. There is also a wide and shal-
low indentation on its posterior margin, at the same
level of the anterior projection. This posterior indenta-
tion of the scapula is delimited by two short posterior
processes on its edges (Figs 15, 16). The inferior pro-
cess defines the superior limit of the attachment of the
m. levator pectoralis to the scapula. Although substan-
tially reduced, this ventral process is topologically sim-
ilar and anchors the m. levator pectoralis, as observed
in members of Dalatiidae (except Dalatias, which lacks
this process), Etmopterus (Etmopteridae) (Fig. 13B)
and Somniosus (Fig. 14B). Due to these similarities,
these ventral processes are considered as homologous
among these taxa. The superior triangular process is
positioned at the upper third of the posterior margin of
the scapula and delimits the base of the scapular pro-
cess. Furthermore, this upper process and the concave
indentation accommodate the ventral bundle of the
hypaxialis musculature, anchoring the scapula to the
lateral body wall. Similar dorsal and ventral triangu-
lar posterior processes defining a shallow indentation
were also found (convergently) in some carcharhini-
forms (S. haeckelii, E. radcliffei, M. griseus) (Fig. 17). In
C. owstonii (Fig. 15B), Zameus (Fig. 15C) and Oxynotus
(Fig. 16C), this indentation is deeper than in other
Somniosidae, Trigonognathus, Scyliorhinus (Fig. 17A),
M. griseus (Fig. 17C) and E. radcliffei (Fig. 17B). This
concavity is not readily visible in juveniles but becomes
more evident late in ontogeny.

Figure 15.  Left lateral views of the scapulae of members of Squaliformes. A, Centroscymnus coelolepis (MNRJ 30224,
female, 580.5-mm TL). B, Centroscymnus owstonii (UERJ A.1460, female, 950-mm TL). C, Zameus squamulosus (HUMZ
143441, female, 579-mm TL). Anterior to left, dorsal to top.

Figure 16.  Left lateral views of the scapulae of members of Squaliformes. A, Scymnodon ringens (BMNH 1991.7.9.686-
690, female, 507-mm TL). B, Scymnodon ichiharai (NMMBP 15843, female, 1317-mm TL). C, Oxynotus bruniensis (USNM
320641, female, 465-mm TL). Anterior to left, dorsal to top.

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 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  11

Figure 17.  Left lateral views of the scapulae of members of Carcharhiniformes. A, Scyliorhinus haeckelii (MZUSP 112024,
male, 385-mm TL). B, Eridacnis radcliffei (CAS 34861, female, 230-mm TL). C, Mustelus griseus (MZUSP uncat., male, 280-
mm TL). Anterior to left, dorsal to top.

DISCUSSION for the anchoring of the m. levator pectoralis (indicated

The scapulae correspond to the dorsal projections
of the scapulocoracoid and provide sites for anchor-
age (pectoral-fin musculature) and insertion (m. cuc-
ullaris) of trunk, branchiomeric and appendicular
muscles, besides attaching the pectoral girdle to the
lateral body musculature (through m. epaxialis and
hypaxialis). The levator muscles of the pectoral fin are
anchored dorsal to the articulation site for the pecto-
ral basals. This anchoring region represents a shallow
or deep posterior indentation, or fossa, with which the
extrinsic pectoral-fin musculature is firmly associated
(Shirai, 1992b, plates 43–45). In most elasmobranchs,
this fossa is shallow and short, delimiting a small
area for the association of the m. levator pectoralis
(lamniforms, hexanchiforms, echinorhiniforms, most
carcharhiniforms) (Figs 3–9, 11, 12). This condition
appears generalized among elasmobranchs. Hybodus,
Hamiltonichthys and Tribodus (Hybodontiformes)
have a similar condition, with a shallow indentation
by a faint indentation dorsal to the pectoral articula-
tion; however, the condition of this musculature is
not reported, see Maisey, 1982: fig. 12, Maisey, 1986:
fig. 5; Maisey, 1989: fig. 14; Lane & Maisey, 2009: figs
9B, 10). Modifications to this pattern were observed
only among the Dalatiidae, Etmopteridae, Oxynotidae,
Somniosidae and Scyliorhinidae (Figs 13–17).
Rays are a clear exception, as the m. levator pectora-
lis shifts to the lateral face of scapula and is anchored
in the region just dorsal of the pectoral condyles,
extending towards the base of the scapular process.
However, members of Rajidae and Arhynchobatidae
have a posterior triangular process (‘posterior corner’,
pcr) that may serve as an additional anchoring point
for this musculature (Fig. 10; coded in red in Figs 18,
19). No other ray taxa have a similar process on the
posterodorsal corner of the scapula. Although this pro-
cess is located dorsal to the metacondyle, somewhat
in a similar position to the ventral triangular process

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 12  J. P. C. B. DA SILVA ET AL.
of Dalatiidae, Etmopteridae, Somniosidae, Oxynotidae,
and some Scyliorhinidae, Proscylliidae, and Triakidae
(see results above) (Figs 13–17), homologizing these
processes is questionable. The scapula of rays has
undergone substantial morphological modifications
related to the shift from axial to pectoral locomotion.
Due to the considerable dorsoventral reduction, the
posterior corner of the scapula of Arhynchobatidae
and Rajidae could be homologous to either the dor-
sal or ventral posterior processes of sharks. However,
these families are recovered as crown groups within
the order Rajiformes (and superorder Batoidea) in
previous phylogenetic hypotheses of relationships
between elasmobranchs (Carvalho, 1996; Shirai, 1996;
Naylor et al., 2012). Therefore, the posterior processes
(pcr) in Arhynchobatidae and Rajidae are interpreted
as not homologous to any of the processes observed
in the posterior surface of the scapula of sharks and
the ‘posterior corner’ would be better interpreted as a
potential synapomorphy, grouping Arhynchobatidae
and Rajidae (McEachran & Compagno, 1979, 1982;
McEachran, 1982, 1984; McEachran & Stehmann,
1984; McEachran & Miyake, 1987; Shirai, 1992b, 1996;
Carvalho, 1996; Carvalho & Maisey, 1996; Naylor
et al., 2012).
Members of Dalatiidae (except Dalatias) and
Somniosus (Somniosidae) (Figs 13, 14; coded in blue
in Figs 18, 19) have a prominent posteroventral tri-
angular process (pvt) defining a deep fossa. Other
shark taxa may have a faint inferior triangular pro-
cess (e.g. Squalus) and eventually an additional dor-
soposterior triangular process (other somniosids,
Oxynotus, Trigonognathus, Mustelus, Scyliorhinus
and Eridacnis) (Figs 15–17; coded in black in Figs 18,
19) at the base of the scapular process. In all cases,
the inferior triangular process delimits the dorsal
boundary where the m. levator pectoralis anchors to
the posterior portion of the scapula. The superior (pdt)
(when present) and inferior (pvt) triangular processes
are also positioned at the edges of a wide and shal-
low concave indentation, delimiting its extension. The
dorsal triangular process and the concave indentation
accommodate the ventral bundle of the m. hypaxi-
alis anchoring the scapula to the lateral body wall.
Onychoselache traquairi (Hybodontiformes) has an
inferior posteroventral process, similar to the observed
in members of Dalatiidae (except Dalatias) and in
Somniosus (Somniosidae) (Coates & Gess, 2007: figs
5B, 9F, 11B; Lane & Maisey, 2009: fig. 11C). As men-
tioned by Coates & Gess (2007), the lowermost third of
the scapula in Onychoselache has a well-defined poste-
rior concavity that might have provided a broad area
of origin for the pectoral-fin levator muscles.
In some shark taxa, the posterior surface of
the scapula is ventrally straight or concave, with
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just the dorsal process on the scapulae (pdt), as
observed in several members of the Carcharhinidae
(Carcharhiniformes) (Figs 11B, C, 12) and also
in Centrophorus (Centrophoridae, Squaliformes)
(Fig. 11A); this condition may be related to a stronger
attachment of the scapulae to the lateral body wall
with the ventral bundle of the hypaxialis musculature.
Tristychius arcuatus, a basal hybodontiform (Maisey,
1989; Coates & Gess, 2007; Lane & Maisey, 2009), has
a condition like the observed in Carcharhinidae and
Centrophorus, although its posterodorsal triangular
process has been interpreted as a ‘posterolateral angle’
(Coates & Gess, 2007: figs 11B; Lane & Maisey, 2009:
figs 9B, 11A), a feature visualized in the scapula of
early chondrichthyans (e.g. cladoselachians, symmorii-
forms and stethacanthids). Nevertheless, even assum-
ing that Tristychius is a hybodontiform, following the
phylogenetic hypothesis of Maisey (1989) and Coates &
Gess (2007), we cannot state whether the posterodor-
sal triangular process present in some extant elasmo-
branchs is homologous to the assumed ‘posterolateral
angle’ of this taxon. According to Coates & Gess (2007),
the presence of a ‘posterolateral angle’ in Tristyschius
(a condition shared with early chondrichthyans) would
correspond to a reversal, as its absence would be one of
the synapomorphies supporting the sister-group rela-
tionship between neoselachians and hybodont sharks.
Additionally, the function of these structures seems
to be different. In extant elasmobranchs, the postero-
dorsal triangular process anchors the scapula to the
lateral body wall; in Tristychius, it apparently serves
as a point of insertion for the dorsal pectoral retractor
(Coates & Gess, 2007).
As noted above, the Hybodontiformes, currently
proposed as the sister group of neoselachians (Maisey,
1989; Maisey, Naylor & Ward 2004; Coates & Gess,
2007; Lane & Maisey, 2009; Pradel et al., 2011), vary
significantly in the posterior surface of the scapula.
Considering this variable scapular morphology and
that the monophyly of the Hybodontiformes is not
consensual, it is difficult to tentatively infer the basal
condition of the scapular morphology for Neoselachii.
This would depend on the phylogenetic position of
controversial taxa (e.g. Tristychius) that would ren-
der different interpretations according to the presence
or absence of monophyletism in hybodontiforms. For
instance, if Tristychius is considered a stem hybodon-
tiform, instead of a basal member of this order, then it
would be possible to putatively indicate the presence
of a posterodorsal triangular process on the scapula
as the basal condition for Euselachii. However, given
the uncertainties of homologizing the posterior process
of the scapula visualized in Tristychius (assumed as a
‘posterolateral angle’) with the posterodorsal triangu-
lar process observed in extant elasmobranch taxa, we
 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  13

Figure 18.  Morphological hypothesis of phylogenetic relationships among extant elasmobranchs modified from Shirai
(1996) with the distribution of the five scapular conditions proposed here (constructed using parsimony and the unordered
characters options in Mesquite).

assume the posterior surface of the scapula without a
ventral and/or dorsal triangular processes is the gen-
eralized condition for neoselachians.
In this study, we propose that the posteroventral tri-
angular process on the scapula is homologous among
Dalatiidae (except Dalatias), Somniosidae, Oxynotidae
and Etmopteridae (Etmopterus and Trigonognathus)
(Figs 13–16). The monophyly of Carcharhiniformes,
supported by several other independent characters
(Compagno, 1988; Shirai, 1996; Naylor et al., 2012), led
us to hypothesize that the posterior ventral (pvt) and
dorsal (pdt) triangular processes found in Scyliorhinus
spp. (Scyliorhinidae), M. griseus (Triakidae) and
E. radcliffei (Proscylliidae) (Fig. 17) are multiple
independent acquisitions within Carcharhiniformes.
Additionally, the distribution of this posterior inferior

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 14  J. P. C. B. DA SILVA ET AL.

Figure 19.  Molecular hypothesis of phylogenetic relationships among extant elasmobranchs modified from Naylor et al.
(2012) with the distribution of the five scapular conditions proposed here (constructed using parsimony and the unordered
characters options in Mesquite).

triangular process on the scapula of Scyliorhinus spp.
(Scyliorhinidae) (Fig. 17A), M. griseus (Triakidae)
(Fig. 17C) and E. radcliffei (Proscylliidae) (Fig. 17B)
is not only variable within genera, but within fami-
lies. Therefore, this character may be helpful to clarify
intergeneric relationships. We did not observe varia-
tion at the species level.
In assessing the distribution of the ventral posterior
process of the scapula in representatives of Dalatiidae,
Somniosidae, Oxynotidae and Etmopteridae, some
interrelationships of Squaliformes can be inferred.
When optimized on previous morphological hypothe-
ses, this scapular character has different phylogenetic
implications. Considering the morphological hypoth-
eses of Shirai (1996), Carvalho (1996) and Adnet
& Cappetta (2001), this pectoral character would
have a single origin in the squaliform clade, unit-
ing Etmopteridae, Somniosidae, Oxynotidae and
Dalatiidae, with a reversion in Dalatias, although rela-
tionships among squaliforms vary among these topolo-
gies (Fig. 18). Molecular phylogenetic proposals would
require further evolutionary steps for this scapular

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 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  15
character. Naylor et al. (2012) hypothesized that this
character appears in the clade uniting Etmopteridae +
[Somniosidae/Oxynotidae + (Squalidae + Dalatiidae)],
but is secondarily lost independently in Squalidae and
Dalatias (Fig. 19). Further homoplasy is required to
account for this character in the carcharhiniform fami-
lies: Scyliorhinidae, Proscylliidae and Triakidae in all
phylogenetic hypotheses (Figs 18, 19).
The additional posteromedial concavity formed by
the dorsal (pdt) and ventral (pvt) triangular pro-
cesses in the scapula could indicate a closer relation-
ship between Oxynotidae and Somniosidae (except
Somniosus), giving further support to the molecu-
lar hypotheses of Naylor et al. (2012) and Straube
et al. (2015), in which Oxynotus appears deeply
nested within Somniosidae. Moreover, the dorsal pro-
cess at the base of the scapular process shared by
Centrophorus (Centrophoridae) (Fig. 11A) and some
members of Carcharhinidae (Figs 11B, C, 12) are not
considered homologous, as these sharks are not closely
related, based on other characters (Compagno, 1973,
1977; Maisey, 1980; Shirai, 1992b, 1996; Carvalho,
1996; Naylor et al., 2012). However, this dorsal process
may indicate a closer relationship of Centrophorus to
Trigonognathus, Oxynotidae (Fig. 16C) and some som-
niosids (all genera except Somniosus) (Figs 15, 16A,
B), as these latter taxa have a short and nearly tri-
angular posterior process on the dorsal third of the
scapula (at the base of the scapular process), along
with the ventral process. The topological and func-
tional similarity of this dorsal process among these
taxa is remarkable, although the optimization of the
dorsal posterior process on previous morphological
and molecular phylogenies would require further
evolutionary steps.
Recently, Silva et al. (2015) proposed a closer rela-
tionship between Somniosidae, Oxynotidae, Dalatiidae
and Centrophoridae based on another pectoral charac-
ter (the presence of a flattened and widened antero-
proximal surface in the first pectoral basal forming
a knob- or a hook-like process). Silva & Carvalho
(2015) also found a single condyle for the articula-
tion of the pectoral basals among Etmopteridae
(except Etmopterus), Somniosidae, Oxynotidae,
Centrophoridae and Dalatiidae as a potential synapo-
morphy uniting these taxa when this pectoral articular
character is optimized on previous morphological and
molecular phylogenetic hypotheses. Accordingly, the
interrelationships inferred from each of these pectoral
characters (i.e. hook-like process, single articular con-
dyle and posterior triangular scapular process) may
differ when considered alone, together these charac-
ters may further support a monophyletic Squaliformes
as proposed by Carvalho (1996), Adnet & Cappetta
(2001) and Naylor et al. (2012) and contrary to Shirai
(1992a, b, 1996).
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Although these characters may be phylogeneti-
cally informative, changes in the arrangement of the
cladogram, the interpretation of the relationships or
the assessment of the homology among the processes
observed in different groups of sharks are only pos-
sible by means of a test of congruence encompassing
a phylogenetic analysis (Hennig, 1966; Patterson,
1982; Farris, 1983; Pinna, 1991; Assis, 2009; Assis &
Rieppel, 2011; Wiley & Lieberman, 2011). Considering
that such potential synapomorphies (mapped on pre-
vious morphological or molecular hypotheses) can
never be shown to be wrong (they are assumed a priori
to be derived), they must be verified as homologous
after morphological or combined phylogenetic analy-
ses incorporating additional characters (see Assis &
Rieppel, 2011, for further discussion).
The new pectoral characters of the scapula pro-
posed, together with previously described pectoral
characters, may aid in elucidating the relationships
between squaliform taxa in future phylogenetic anal-
yses. The importance of the scapular characters for
the relationships among galeomorph taxa bearing
the dorsal and ventral posterior processes (Eridacnis,
Mustelus and Scyliorhinus) must be investigated fur-
ther. The distribution in the proposed paraphyletic
carcharhiniform families Scyliorhinidae, Proscylliidae
and Triakidae (Shirai, 1996; Naylor et al. 2012) could
indicate a closer relationship among the species S. hae-
ckelii (Scyliorhinidae), E. radcliffei (Proscylliidae) and
M. griseus (Triakidae) than to other congeneric spe-
cies, reflecting not only the paraphyletism of these
carcharhiniform families, but even of some of its
included genera, so far considered monophyletic (e.g.
Scyliorhinus). Considering the infrequent presence
of these characters among carcharhiniforms (present
only in some species within each genus), more species
must be studied to corroborate their significance.
CONCLUSIONS
1. The posterior surface of the scapula varies mor-
phologically, with potential phylogenetic informa-
tion. We propose that the generalized condition of
elasmobranch scapula has a posteroventral sur-
face with a shallow or deep indentation or fossa, in
which the m. levator pectoralis (lp) is firmly asso-
ciated. This same condition is present in the fos-
sil taxa Hybodus, Hamiltonichthys and Tribodus
(Hybodontiformes).
2. Etmopteridae, Somniosidae, Oxynotidae and
Dalatiidae (excepting Dalatias) share a distinct tri-
angular process (pvt) in the ventral third surface
of the scapula, which provides additional site for
the origin of the m. levator pectoralis. This process
 16  J. P. C. B. DA SILVA ET AL.
could be interpreted as putative synapomorphy
grouping these taxa.
3. Oxynotus (Oxynotidae), Zameus, Centroscymnus
spp., Scymnodon spp., Scymnodalatias,
Centroselachus, Proscymnodon (Somniosidae) and
Trigonognathus (Etmopteridae) share a unique
posterior surface of the scapula, with both ven-
tral (pvt) and dorsal (pdt) processes within
Squaliformes, forming a posteromedial concavity
for the axial musculature anchor. The pvt, pdt and
the posteromedial concavity observed in S. haecke-
lii (Scyliorhinidae), E. radcliffei (Proscylliidae) and
M. griseus (Triakidae) are interpreted as homoplas-
tic occurrences.
4. The posterior corner (pcr) observed in Rajidae and
Arhynchobatidae is not homologous to any of the
posterior processes in the scapula of squaliform
and carcharhiniform sharks. Instead, this process
is interpreted as a unique shared characteristic
between these two families.
ACKNOWLEDGEMENTS
J. Figueiredo, A. Datovo and M. Gianeti (MZUSP); U.
Gomes and H. Santos (UERJ); M. Britto (MNRJ); J.
Sparks, R. Schelly, R. Arindell and B. Brown (AMNH);
J. Williams, R. Vari, J. Finnan, J. Clayton, S. Raredon,
K. Murphy and D. Pitassy (USNM); D. Catania, L.
Rocha, J. Fong, M. Hoang, B. Santos and M. Bernal
(CAS); L. Page and R. Robins (UF); K. Hartel and A.
Williston (MCZ); M. Yabe and T. Kawai (HUMZ); O.
Crimmen and J. Maclaine (BMNH); G. Shinohara, M.
Nakae, F. Tashiro and E. Katayama (NSMT); S. Tanaka
(University of Tokai); and H. Ho (NMMBP) are sin-
cerely thanked for providing access to specimens cru-
cial to this paper and for their hospitality and support.
This project was funded by the Fundação de Amparo
à Pesquisa do Estado de São Paulo (FAPESP) through
grants to the J.P.C.B.S. (2010/52677-6, 2012/22692-
9), D.F.B.V. (2012/07712-3, 2013/13137-4) and M.R.C.
(2012/09877-0, 2012/02349-8, 2012/05391-5) authors;
M.R.C. is also grateful for funding from the Conselho
Nacional de Desenvolvimento Científico e Tecnológico
(CNPq 304615/2011-0). D.F.B.V. is currently funded
by the Graduate Support Package of the Virginia
Institute of Marine Science.
REFERENCES
Adnet S, Cappetta H. 2001. A palaeontological and phylo-
genetical analysis of squaliform sharks (Chondrichthyes:
Squaliformes) based on dental characters. Lethaia 34:
234–248.
© 2017 The Linnean Society of London, Zoological Journal of the Linnean Society, 2017, XX, 1–17
Downloaded from https://academic.oup.com/zoolinnean/article-abstract/doi/10.1093/zoolinnean/zlx051/4093063/Phylogenetic-inferences-on-the-systematics-of
by guest
on 24 August 2017
Assis LCS. 2009. Coherence, correspondence, and the renais-
sance of morphology in phylogenetic systematics. Cladistics
25: 528–544.
Assis LCS, Rieppel O. 2011. Are monophyly and synapomor-
phy the same or different? Revisiting the role of morphology
in phylogenetics. Cladistics 27: 94–102.
Cappetta H. 2012. Chondrichthyes. Mesozoic and Cenozoic
Elasmobranchii: teeth. In: Schultze HP, ed. Handbook of pale-
oichthyology, Vol. 3E. Munich: Verlag Dr. Friedrich Pfeil, 1–512.
Carvalho MR. 1996. Higher-lever elasmobranch phylogeny,
basal squaleans, and paraphyly. In: Stiassny MLJ, Parenti
LR, Johnson GD, eds. Interrelationships of fishes. New York:
Academic Press, 35–62.
Carvalho MR, Maisey JG. 1996. Phylogenetic relationships
of the Late Jurassic shark Protospinax Woodward 1919
(Chondrichthyes: Elsmobranchii). In: Arratia G, Viohl G, eds.
Mesozoic fishes – systematics and paleoecology. München:
Verlag Dr. Friedrich Pfeil, 9–46.
Coates MI, Gess RW. 2007. A new reconstruction of
Onychoselache traquairi, comments on early chondrichthyan
pectoral girdles and hybodontiform phylogeny. Paleontology
50: 1421–1446.
Compagno LJV. 1973. Interrelationships of living elasmo-
branchs. In: Greenwood PH, Miles RS, Patterson C, eds.
Interrelationships of fishes. New York: Academic Press,
15–61.
Compagno LJV. 1977. Phyletic relationships of living sharks
and rays. American Zoologist 17: 303–322.
Compagno LJV. 1988. Sharks of the order Carcharhiniformes.
Princeton: Princeton University Press.
Compagno LJV. 1999. Endoskeleton. In: Hamlett WC, ed.
Sharks, skates, and rays, the biology of elasmobranch fishes.
Baltimore: John Hopkins University Press, 69–92.
Daniel JF. 1934. The elasmobranch fishes, 3rd edn. Berkeley:
University of California Press.
Dingerkus G, Uhler LD. 1977. Enzyme clearing of alcian
blue stained whole small vertebrates for demonstration of
cartilage. Stain Technology 52: 229–232.
Farris JS. 1983. The logical basis of phylogenetic analy-
sis. In: Platnick NI, Funk VA, eds. Advanced in cladistics.
Proceedings of the second meeting of the Willi Hennig Society,
Vol. 2. New York: Columbia University Press, 7–36.
Goto T, Nishida K, Nakaya K. 1999. Internal morphology and
function of paired fins in the epaulette shark, Hemiscyllium
ocellatum. Ichthyological Research 46: 281–287.
Gudo M, Homberger DM. 2002. The functional morphol-
ogy of the pectoral fin girdle of the spiny dogfish (Squalus
acanthias): implications for the evolutionary history of the
pectoral girdle of vertebrates. Senckenbergiana Lethaea 82:
241–252.
Hennig W. 1966. Phylogenetic systematics. Urbana: University
of Illinois Press.
Lane JA, Maisey JG. 2009. Pectoral anatomy of Tribodus
limae (Elasmobranchii: Hybodontiformes) from the Lower
Cretaceous of northeastern Brazil. Journal of Vertebrate
Paleontology 29: 25–38.
Liem KF, Summers AP. 1999. Gross anatomy and func-
tional morphology of the muscles. In: Hamlett WC, ed.
 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  17
Sharks, skates, and rays, the biology of elasmobranch fishes.
Baltimore: John Hopkins University Press, 93–114.
Maddison WP, Maddison DR. 2016. Mesquite: a modular
system for evolutionary analysis. Version 3.11. Available at:
http://mesquiteproject.org
Maia AMR, Wilga CAD, Lauder GV. 2012. Biomechanics of
locomotion in sharks, rays, and chimaeras. In: Carrier JC,
Musick JA, Heithaus MR, eds. Biology of sharks and their
relatives, 2nd edn. Boca Raton: CRC Press, 125–151.
Maisey JG. 1980. An evaluation of jaw suspension in sharks.
American Museum Novitates 2706: 1–17.
Maisey JG. 1982. The anatomy and interrelationships of
Mesozoic hybodont sharks. American Museum Novitates
2724: 1–48.
Maisey JG. 1986. Anatomical revision of the fossil shark
Hybodus fraasi (Chondrichthyes: Elasmobranchii). American
Museum Novitates 2857: 1–16.
Maisey JG. 1989. Hamiltonichthys mapesi, g. & sp. nov.
(Chondrichthyes; Elasmobranchii), from the Upper
Pennsylvanian of Kansas. American Museum Novitates
2931: 1–42.
Maisey JG, Naylor GJP, Ward DJ. 2004. Mesozoic elasmo-
branchs, neoselachian phylogeny and the rise of modern elas-
mobranch diversity. In: Arratia G, Tintori A, eds. Mesozoic
fishes 3 – systematics, paleoenvironments and biodiversity.
München: Verlag Dr. Friedrich Pfeil, 17–56.
McEachran JD. 1982. Revision of the South American skate
genus Sympterygia (Elasmobranchii: Rajiformes). Copeia
1982: 867–890.
McEachran JD. 1984. Anatomical investigations of the New
Zealand skates Bathyraja asperula and B. spinifera, with
an evaluation of their classification within the Rajoidei
(Chondrichthyes). Copeia 1984: 45–58.
McEachran JD, Compagno LJV. 1979. A further descrip-
tion of Gurgesiella furvescens with comments on the inter-
relationships of Gurgesiellidae and Pseudorajidae (Pisces,
Rajoidei). Bulletin of Marine Science 29: 530–553.
McEachran JD, Compagno LJV. 1982. A new species of
skate from the western Indian Ocean, with comments on
the status of Raja (Okamejei) (Elasmobranchii: Rajiformes).
Proceedings of the Biological Society of Washington 95:
440–450.
McEachran JD, Dunn K. 1998. Phylogenetic analysis of
skates, a morphologically conservative clade of elasmo-
branchs (Chondrichthyes: Rajidae). Copeia 1998: 271–290.
McEachran JD, Miyake T. 1987. A new species of skate of the
genus Breviraja from off Nova Scotia, with comments on the
status of Breviraja and Neoraja (Chondrichthys, Rajoidei).
Copeia 1987: 409–417.
McEachran JD, Stehmann M. 1984. A new species of skate,
Neoraja carolinensis, from off the southeastern United States
(Elasmobranchii: Rajoidei). Proceedings of the Biological
Society of Washington 97: 724–735.
Naylor GJP, Caira JN, Jensen K, Rosana KAM, Straube N,
Lakner C. 2012. Elasmobranch phylogeny: a mitochondrial
© 2017 The Linnean Society of London, Zoological Journal of the Linnean Society, 2017, XX, 1–17
Downloaded from https://academic.oup.com/zoolinnean/article-abstract/doi/10.1093/zoolinnean/zlx051/4093063/Phylogenetic-inferences-on-the-systematics-of
by guest
on 24 August 2017
View publication stats
estimate based on 595 species. In: Carrier JC, Musick JA,
Heithaus MR, eds. Biology of sharks and their relatives, 2nd
edn. Boca Raton: CRC Press, 31–56.
Patterson C. 1982. Morphological characters and homology.
In: Joysey KA, Friday AE, eds. Problems of phylogenetic
reconstruction. London: Academic Press, 21–74.
Pinna MCC. 1991. Concepts and tests of homology in the cla-
distic paradigm. Cladistics 7: 367–394.
Pradel A, Tafforeau P, Maisey JG, Janvier P. 2011. A new
paleozoic Symmoriiformes (Chondrichthyes) from the late
Carboniferous of Kansas (USA) and cladistic analysis of
early chondrichthyans. PLoS ONE 6: e24938.
Rosenberger LJ. 2001. Pectoral fin locomotion in batoid
fishes: undulation versus oscillation. The Journal of
Experimental Biology 204: 379–394.
Shirai S. 1992a. Phylogenetic relationships of the angel
sharks, with comments on elasmobranch phylogeny
(Chondrichthyes, Squatinidae). Copeia 1992: 505–518.
Shirai S. 1992b. Squalean phylogeny: a new framework of
“Squaloid” sharks and related taxa. Sapporo: Hokkaido
University Press.
Shirai S. 1996. Phylogenetic interrelationships of neoselachi-
ans (Chondrichthyes: Euselachii). In: Stiassny MLJ, Parenti
LR, Johnson GD, eds. Interrelationships of fishes. New York:
Academic Press, 9–34.
Silva JPCB. 2014. Phylogeny of the major groups of
Chondrichthyes based on the comparative anatomy of the
skeleton of the paired fins and girdles. Unpublished Ph.D.
Thesis, Instituto de Biociências, Universidade de São Paulo.
Silva JPCB, Carvalho MR. 2015. Morphology and phyloge-
netic significance of the pectoral articular region in elasmo-
branchs (Chondrichthyes). Zoological Journal of the Linnean
Society 175: 525–568.
Silva JPCB, Vaz DFB, Carvalho MR. 2015. Systematic
implications of the anterior pectoral basals in squaliform
sharks (Chondrichthyes: Elasmobranchii). Copeia 103:
874–885.
Straube N, Li C, Claes JM, Corrigan S, Naylor GJ. 2015.
Molecular phylogeny of Squaliformes and first occurrence of
bioluminescence in sharks. BMC Evolutionary Biology 15:
162.
Tomita T, Tanaka S, Sato K, Nakaya K. 2014. Pectoral fin of
the megamouth shark: skeletal and muscular systems, skin
histology, and functional morphology. PLoS ONE 9: 1–8.
Wiley EO, Lieberman BS. 2011. Phylogenetics: the theory
and practice of phylogenetic systematics, 2nd edn. Hoboken:
Wiley-Blackwell.
Wilga CD, Lauder GV. 2001. Functional morphology of the
pectoral fins in bamboo sharks, Chiloscyllium plagiosum:
benthic vs. pelagic station-holding. Journal of Morphology
249: 195–209.
Wilga CAD, Lauder GV. 2004. Biomechanics of locomotion
in sharks, rays and chimeras. In: Carrier JC, Musick JA,
Heithaus MR, eds. Biology of sharks and their relatives. Boca
Raton: CRC Press, 139–164.