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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: [email protected] taxa (e.g. McEachran & Compagno, 1979, 1982; Shirai,

© 2017 The Linnean Society of London, Zoological Journal of the Linnean Society, 2017, XX, 1–17 1

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 2  J. P. C. B. DA SILVA ET AL.

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

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 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-

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

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 4  J. P. C. B. DA SILVA ET AL.

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
Figure 2.  Left lateral view of the scapula of Somniosus process. There is also an indentation in the lower por-
rostratus (MZUSP uncat., male, 1319-mm TL) depicting its tion of the scapulae anchoring the m. levator pectoralis
associated pectoral musculature. Anterior to left, dorsal to (lp). This condition is clear in L. nasus and I. oxyrin-
top. chus (Lamnidae) (Fig. 4B).
All representatives of Hexanchiformes (Figs 7A–C)
have a pattern that resembles most carcharhini-
Posterior margin of the scapula (scl) with a forms, except for the reduced diazonal foramen.
ventral indentation and lacking a posterior
The scapula is only enlarged basally and tapers
process (pdt and/or pvt)
dorsally, culminating in a filiform and poorly calci-
(coded in white in Figs 18, 19) fied scapular process (detached from the scapula in
This condition was observed in most elasmobranch C. anguineus). There is a posterior flattened area
taxa (Figs 3–9). The posterior margin of the scapula immediately above the pectoral articulation anchor-
(scl) is smooth and lacks any sort of process on its sur- ing the m. levator pectoralis. In E. cookei (Fig. 8A),
face. The posterior surface of the scapula varies from the scapula is greatly enlarged at its base and tapers
straight to sinuous; when sinuous, the posterior mar- distally, ending in a nearly rhomboid scapular pro-
gin can be either concave, convex or a combination of cess. The posterior margin of the scapula is slightly
both. The ventral portion of the posterior margin of convex and lacks any process. However, a nearly oval,
the scapulae has an indentation (idt), varying from flattened area in the ventral portion of the posterior
faint (e.g. Heterodontiformes) (Fig. 3B) to prominent margin serves as an anchoring point for the m. leva-
(e.g. Lamnidae) (Fig. 4B). Although this indentation tor pectoralis. Representatives of Squaliformes, such
is remarkable in some groups, it does not form a dis- as Deania (Centrophoridae) (Fig. 9A) and Dalatias
tinct posteriorly directed process (as observed in other (Dalatiidae) (Fig. 8B), also have a continuous poste-
shark taxa; see below). The surface of this indentation rior scapular surface, lacking any sort of posterior
is slightly flattened and serves as an anchoring point processes. In these species, the scapula is basally
for the m. levator pectoralis. thick and tapers somewhat towards its tip, ending
In Heterodontiformes and Orectolobiformes (Fig. 3B, in a broadly pointed scapular process. In Squatina
C), the scapula is tall (slightly shorter than the cora- (Fig. 9B), the scapula is tall, stout and tapers
coid bar), stout and has similar proportions through its faintly from its base towards its tip, terminating
entire extension, except distally, where it tapers and in a scapular process that varies from rectangular
forms a rhomboidal scapular process (scp). Basally, to triangular. The anterior and posterior margins

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 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) (Arhynchobatidae) (Fig. 10C), a nearly triangular
In rays, the scapula is highly variable, but vis- posterior process is at the posterodorsal corner of the
ibly anteroposteriorly expanded and dorsoventrally scapula (‘rear corner’ of McEachran & Compagno,
short when compared to sharks. The extension of the 1979, 1982; McEachran & Stehmann, 1984). This pos-
scapular process varies from short (one fourth of the terior process (pcr) is posterodorsal to the pectoral
dorsoventral scapular length; e.g. Rajiformes) to tall condyles and fenestrae (Fig. 10).
(equal to or greater than the dorsoventral scapular The homology of the posterior corner is uncer-
length) in Torpediniformes, Rhinopristiformes and tain. It is topologically similar to the inferior process
some Myliobatiformes (e.g. Dasyatidae, Urolophidae, observed in some shark taxa. However, due to its
Potamotrygonidae). The anterior and posterior sur- restricted distribution (present only in rajiform fami-
faces of the scapula vary from faintly to strongly lies), we are regarding the posterior process of skates
convex and host the procondyle and metacondyle, as non-homologous to the inferior process observed
respectively. In D. mennii (Rajidae) (Fig. 10B), 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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A single posterodorsal process (pdt) on the Carcharhinidae. The scapula of C. granulosus is wide
dorsal third of the scapula or at the base of the at its base and tapers toward the ventral origin of both
scapular process (coded in yellow in Figs 18, 19) anterior and posterior processes. The scapular process
In this condition, the scapula is basally expanded and is basally wide (wider than the dorsal portion of the
tapered dorsally, terminating in an acute and eventu- scapula), forming a rhomboidal distal tip. The scapula
ally posteriorly curved scapular process (e.g. G. cuvier) is nearly straight posteriorly, being convex only at the
(Fig. 11B). Additionally, the anterior margin of the level of the posterior process. A small diazonal foramen
scapula is concave and its posterior margin convex. pierces the base of the scapula just anterior to the pec-
The base of the scapula has a wide circular diazonal toral condyle.
foramen anterior to the pectoral articular region. Most of the representatives of Carcharhinidae have
Centrophorus granulosus (Centrophoridae) (Fig. 11A) a filiform scapular process, with a rounded projec-
has a similar posterior process in the upper third of the tion (pdt) on the base of the posterior margin (e.g.
scapula at the base of the scapular process (although Rhizoprionodon spp., P. glauca, G. cuvier, Carcharhinus
there is no clear distinction between the scapular pro- spp., S. laticaudus). The shape of this projection var-
cess and scapula). However, the anterior margin of ies from wide, shallow and rounded (Fig. 11B, C), to
C. granulosus has an additional symmetrical anterior pointed and nearly triangular (e.g. S. laticaudus)
process on the anterior margin of the scapula that is (Fig. 12B). However, it may be absent in some repre-
not as arched and does not taper distally as observed in 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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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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(Zameus, C. coelolepis, C. owstonii, Oxynotus, S. rin- and Somniosus (Fig. 14B). Due to these similarities,
gens, S. ichiharai, Scyliorhinus spp.) (Figs 15–17), the these ventral processes are considered as homologous
scapula presents a subtle anteroposterior compression among these taxa. The superior triangular process is
at its proximal half. The scapula is also oriented poste- positioned at the upper third of the posterior margin of
riorly to some extent and has a concave anterior mar- the scapula and delimits the base of the scapular pro-
gin and convex posterior margin. The anterior margin cess. Furthermore, this upper process and the concave
of the scapula has a wide and shallow convex projection indentation accommodate the ventral bundle of the
at its medial portion. There is also a wide and shal- hypaxialis musculature, anchoring the scapula to the
low indentation on its posterior margin, at the same lateral body wall. Similar dorsal and ventral triangu-
level of the anterior projection. This posterior indenta- lar posterior processes defining a shallow indentation
tion of the scapula is delimited by two short posterior were also found (convergently) in some carcharhini-
processes on its edges (Figs 15, 16). The inferior pro- forms (S. haeckelii, E. radcliffei, M. griseus) (Fig. 17). In
cess defines the superior limit of the attachment of the C. owstonii (Fig. 15B), Zameus (Fig. 15C) and Oxynotus
m. levator pectoralis to the scapula. Although substan- (Fig. 16C), this indentation is deeper than in other
tially reduced, this ventral process is topologically sim- Somniosidae, Trigonognathus, Scyliorhinus (Fig. 17A),
ilar and anchors the m. levator pectoralis, as observed M. griseus (Fig. 17C) and E. radcliffei (Fig. 17B). This
in members of Dalatiidae (except Dalatias, which lacks concavity is not readily visible in juveniles but becomes
this process), Etmopterus (Etmopteridae) (Fig. 13B) 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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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

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

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

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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 supported by several other independent characters
ventral and/or dorsal triangular processes is the gen- (Compagno, 1988; Shirai, 1996; Naylor et al., 2012), led
eralized condition for neoselachians. us to hypothesize that the posterior ventral (pvt) and
In this study, we propose that the posteroventral tri- dorsal (pdt) triangular processes found in Scyliorhinus
angular process on the scapula is homologous among spp. (Scyliorhinidae), M. griseus (Triakidae) and
Dalatiidae (except Dalatias), Somniosidae, Oxynotidae E. radcliffei (Proscylliidae) (Fig. 17) are multiple
and Etmopteridae (Etmopterus and Trigonognathus) independent acquisitions within Carcharhiniformes.
(Figs 13–16). The monophyly of Carcharhiniformes, Additionally, the distribution of this posterior inferior

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

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 SCAPULAR MORPHOLOGY IN ELASMOBRANCHS  15

character. Naylor et al. (2012) hypothesized that this Although these characters may be phylogeneti-
character appears in the clade uniting Etmopteridae + cally informative, changes in the arrangement of the
[Somniosidae/Oxynotidae + (Squalidae + Dalatiidae)], cladogram, the interpretation of the relationships or
but is secondarily lost independently in Squalidae and the assessment of the homology among the processes
Dalatias (Fig. 19). Further homoplasy is required to observed in different groups of sharks are only pos-
account for this character in the carcharhiniform fami- sible by means of a test of congruence encompassing
lies: Scyliorhinidae, Proscylliidae and Triakidae in all a phylogenetic analysis (Hennig, 1966; Patterson,
phylogenetic hypotheses (Figs 18, 19). 1982; Farris, 1983; Pinna, 1991; Assis, 2009; Assis &
The additional posteromedial concavity formed by Rieppel, 2011; Wiley & Lieberman, 2011). Considering
the dorsal (pdt) and ventral (pvt) triangular pro- that such potential synapomorphies (mapped on pre-
cesses in the scapula could indicate a closer relation- vious morphological or molecular hypotheses) can
ship between Oxynotidae and Somniosidae (except never be shown to be wrong (they are assumed a priori
Somniosus), giving further support to the molecu- to be derived), they must be verified as homologous
lar hypotheses of Naylor et al. (2012) and Straube after morphological or combined phylogenetic analy-
et al. (2015), in which Oxynotus appears deeply ses incorporating additional characters (see Assis &
nested within Somniosidae. Moreover, the dorsal pro- Rieppel, 2011, for further discussion).
cess at the base of the scapular process shared by The new pectoral characters of the scapula pro-
Centrophorus (Centrophoridae) (Fig. 11A) and some posed, together with previously described pectoral
members of Carcharhinidae (Figs 11B, C, 12) are not characters, may aid in elucidating the relationships
considered homologous, as these sharks are not closely between squaliform taxa in future phylogenetic anal-
related, based on other characters (Compagno, 1973, yses. The importance of the scapular characters for
1977; Maisey, 1980; Shirai, 1992b, 1996; Carvalho, the relationships among galeomorph taxa bearing
1996; Naylor et al., 2012). However, this dorsal process the dorsal and ventral posterior processes (Eridacnis,
may indicate a closer relationship of Centrophorus to Mustelus and Scyliorhinus) must be investigated fur-
Trigonognathus, Oxynotidae (Fig. 16C) and some som- ther. The distribution in the proposed paraphyletic
niosids (all genera except Somniosus) (Figs 15, 16A, carcharhiniform families Scyliorhinidae, Proscylliidae
B), as these latter taxa have a short and nearly tri- and Triakidae (Shirai, 1996; Naylor et al. 2012) could
angular posterior process on the dorsal third of the indicate a closer relationship among the species S. hae-
scapula (at the base of the scapular process), along ckelii (Scyliorhinidae), E. radcliffei (Proscylliidae) and
with the ventral process. The topological and func- M. griseus (Triakidae) than to other congeneric spe-
tional similarity of this dorsal process among these cies, reflecting not only the paraphyletism of these
taxa is remarkable, although the optimization of the carcharhiniform families, but even of some of its
dorsal posterior process on previous morphological included genera, so far considered monophyletic (e.g.
and molecular phylogenies would require further Scyliorhinus). Considering the infrequent presence
evolutionary steps. of these characters among carcharhiniforms (present
Recently, Silva et al. (2015) proposed a closer rela- only in some species within each genus), more species
tionship between Somniosidae, Oxynotidae, Dalatiidae must be studied to corroborate their significance.
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 CONCLUSIONS
(2015) also found a single condyle for the articula-
tion of the pectoral basals among Etmopteridae 1. The posterior surface of the scapula varies mor-
(except Etmopterus), Somniosidae, Oxynotidae, phologically, with potential phylogenetic informa-
Centrophoridae and Dalatiidae as a potential synapo- tion. We propose that the generalized condition of
morphy uniting these taxa when this pectoral articular elasmobranch scapula has a posteroventral sur-
character is optimized on previous morphological and face with a shallow or deep indentation or fossa, in
molecular phylogenetic hypotheses. Accordingly, the which the m. levator pectoralis (lp) is firmly asso-
interrelationships inferred from each of these pectoral ciated. This same condition is present in the fos-
characters (i.e. hook-like process, single articular con- sil taxa Hybodus, Hamiltonichthys and Tribodus
dyle and posterior triangular scapular process) may (Hybodontiformes).
differ when considered alone, together these charac- 2. Etmopteridae, Somniosidae, Oxynotidae and
ters may further support a monophyletic Squaliformes Dalatiidae (excepting Dalatias) share a distinct tri-
as proposed by Carvalho (1996), Adnet & Cappetta angular process (pvt) in the ventral third surface
(2001) and Naylor et al. (2012) and contrary to Shirai of the scapula, which provides additional site for
(1992a, b, 1996). the origin of the m. levator pectoralis. This process

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could be interpreted as putative synapomorphy Assis LCS. 2009. Coherence, correspondence, and the renais-
grouping these taxa. sance of morphology in phylogenetic systematics. Cladistics
3. Oxynotus (Oxynotidae), Zameus, Centroscymnus 25: 528–544.
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