First record of a bicephalic embryo of smalltail shark
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Journal of Fish Biology (2013) 82, 1753–1757
doi:10.1111/jfb.12102, available online at wileyonlinelibrary.com
First record of a bicephalic embryo of smalltail shark
Carcharhinus porosus
L. A. Muñoz-Osorio*, P. A. Mejía-Falla and A. F. Navia
Fundación colombiana para la investigación y conservación de tiburones y rayas, SQUALUS.
Carrera 79 No. 6-37 Cali, Colombia
(Received 3 May 2012, Accepted 14 February 2013)
This study reports the first bicephalic embryo of smalltail shark Carcharhinus porosus, which
was removed from a pregnant female in coastal waters of the tropical eastern Pacific Ocean. The
observation suggested that although the individual’s body was well formed, the malformation of the
head would have affected it survival. © 2013 The Authors
Journal of Fish Biology © 2013 The Fisheries Society of the British Isles
Key words: abnormality; deformities; X-ray; Pacific Ocean; Colombia; Elasmobranchii.
The smalltail shark Carcharhinus porosus (Ranzani 1839) is distributed in the east-
ern Pacific Ocean, from the southern Gulf of California to Peru and in the western
Atlantic Ocean from the northern Gulf of Mexico to Uruguay (Menni & Lucifora,
2007), including the Caribbean Sea (Compagno et al ., 1995; Compagno, 2002;
Robertson & Allen, 2008). This species is common in shallow coastal waters (to
36 m) over muddy bottoms of continental shelves and estuarine habitats (Compagno,
2003). Carcharhinus porosus is by-catch in artisanal and industrial fishing along
the Colombian Caribbean and Pacific coasts, where its meat is sold commercially
(Caldas et al ., 2009; Navia et al ., 2009; Navia & Mejía-Falla, 2011).
Reports on morphological abnormalities for elasmobranchs include: albinism
(Joseph, 1961; Talent, 1973; de Jesus-Roldán, 1990; Ben-Brahim et al ., 1998;
Clark, 2002; Ferreira & Góes, 2002; Rider et al ., 2002; Bottaro et al ., 2005; Saidi
et al ., 2006; Sandoval-Castillo et al ., 2006), anophthalmy (Gomes et al ., 1991),
deformities in the axial skeleton (Springer, 1960; Bensam, 1965; Mancini et al .,
2006), deformities in pectoral fin development, i .e. not fused to the head (in batoids)
(Templeman, 1965; Honma & Sugihara, 1971; Lamilla et al ., 1995; Rosa et al .,
1996; Oldfield, 2005; Escobar-Sánchez et al ., 2009; Mejía-Falla et al ., 2011) and
bicephalia (Castro-Aguirre & Torres-Villegas, 1979; Bornatowski & Abilhoa, 2009).
This article reports the first case of bicephalia in the smalltail shark C . porosus.
*Author to whom correspondence should be addressed. Tel.: +57 2 370589; email: lmunoz@squalus.org
1753
© 2013 The Authors
Journal of Fish Biology © 2013 The Fisheries Society of the British Isles1754 L . A . M U Ñ O Z - O S O R I O E T A L .
Gill openings Pelvic fin Eyes
(a) (b)
Tail Heads Pectoral fin
Gill openings Eyes
First dorsal fin Second dorsal
fin
Pectoral fin
(c) Mouth
Eyes
Second dorsal Tail
fin
Mouth
Fig. 1. Bicephalic embryo of Carcharhinus porosus: (a) dorsal, (b) right lateral and (c) ventral view.
A pregnant female C . porosus was captured in Pizarro, Chocó, in the central
Pacific Ocean coast of Colombia (77◦ 24 N; 5◦ 03 W) on 23 May 2008; its
embryo was an abnormal male, which was measured, photographed and subse-
quently radiographed using mammography equipment (CGR Senographe 500 T;
www3gehealthcare.com/en/Global_Gateway). The identification of the species
was based on Compagno et al . (1995); Compagno (2003) and Robertson &
Allen (2008).
The male embryo was 28 cm in total length, 22·5 cm in standard length and
weighed 109 g. This embryo had a single body with two dorsal and pectoral fins, one
anal fin and one caudal fin. Two heads, however, originated anterior to the gills, each
one with a mouth, a single gill opening, a pair of eyes, but only one shared ocular
socket (Fig. 1). An X-radiograph showed the attachment site of the two heads to be in
the back of the skull (Fig. 2). An important feature of this embryo is that the body was
supported by a well-developed vertebral column but it had another under-developed
vertebral column, indicating that this specimen was a conjoined twin.
Bicephaly has been found in shark species such as Squalus acanthias L.
1758 (Bosinceano, 1934), Squalus blainville (Risso 1826) (Lozano-Cabo, 1945),
Rhizoprionodon acutus (Rüppell 1837) (Gopalan, 1971), Carcharhinus perezi (Poey
1876) (Bonfil, 1989), Prionace glauca (L. 1758) (Goto et al ., 1981; Mancini et al .,
2006; Galván-Magaña et al ., 2011) and Galeorhinus galeus (L. 1758) (Delpiani
et al ., 2011).
Conjoined monozygotic twins are the result of an aberration in development, in
which one twin derived from a single fertilized ovum is not completely separated due
to a partial duplication that occurs in early stages of intra-uterine life (Lugones-Botell
et al ., 1999). Conjoined twins are very rare in sharks and could be explained by the
relationship between the number of embryos and uterine size (Galván-Magaña et al .,
2011), parasitic infections, arthritis, tumours or poor nutrition, and even unfavourable
© 2013 The Authors
Journal of Fish Biology © 2013 The Fisheries Society of the British Isles, Journal of Fish Biology 2013, 82, 1753–1757F I R S T R E C O R D O F A B I C E P H A L I C C A R C H A R H I N U S P O RO S U S 1755
Nostrils
Upper jaw
Joining site
of the two
heads
Lower jaw
Division in
column
Second
column
atrophied
Fig. 2. Ventral view X-radiogram of the bicephalic embryo of Carcharhinus porosus, indicating the vertebral
column bifurcation, the atrophied second column as well as the attachment site of the two heads in the
back of the skull.
environmental conditions such as pollution (Heupel et al ., 1999; Mancini et al ., 2006;
Saidi et al ., 2006; Delpiani et al ., 2011).
Despite this abnormality, intrauterine growth of the individual was apparently
not affected as it was a near-term foetus (Lessa & Santana, 1998). Although the
cause of the abnormality of this embryo is unknown, this individual would probably
not survive long after birth, due to difficulties of swimming, feeding and evading
predators with this condition (Bengtsson, 1979; Mancini et al ., 2006).
The authors would like to thank H. López who provided the embryo and J. Muñoz who
collaborated with the X-radiograms; the X-ray section of the Red Cross for providing equip-
ment. P. Sargent and V. Ramirez reviewed the English manuscript. The project was co-funded
by the PADI Foundation and the Initiative for Threatened Species (IEA fellowships).
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