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Several morphological abnormalities have been reported in sharks (Subclass: Selachii) in different marine ecoregions around the world. This reports include albinism (e.g., Clark, 2002; Saïdi et al., 2006; Bottaro et al., 2008; Escobar-Sánchez et al., 2014), bicephaly (e.g., Galván-Magaña et al., 2011; Wagner et al., 2013), diprosopia (e.g., Mancini et al., 2006; Hevia-Hormazábal et al., 2011; Driggers et al., 2012), deformities in axial skeleton (e.g., Pastore & Prato, 1989; Heupel et al., 1999; Mancini et al., 2006), mummification (e.g., Rosa-Molinar et al., 1983; Sandoval-Castillo & Villavicencio-Garay-Zar, 2008) and even cyclopia (Bejarano-Álvarez & Galván-Magaña, 2013). Blue shark (Prionace glauca) is the shark species with the highest number of anomalies reported, which have been described by different authors (e.g., Goto et al., 1981; Mancini et al., 2006; Galván-Magaña et al., 2011; Hevia-Hormazábal et al., 2011; Bejarano-Álvarez et al., 2013; Ehemann et al., 2016; Rodríguez-Romero et al., 2018; Ramírez-Amaro et al., 2019).
The blue shark is one of the most abundant shark species in temperate, subtropical and tropical seas (Fischer et al., 1995; Nakano & Stevens, 2008; Castro, 2010). It is a pelagic species mainly distributed from the epipelagic zone to depths of about 350 m, even reached 1,000 m (Da Silva et al., 2010; Campana et al., 2011). This shark is placental viviparous, producing litters averaging about 35 pups after a gestation period of 9-12 months and the size at birth is between 350 and 500 mm total length (Fischer et al., 1995; Camhi et al., 1998; Nakano & Stevens, 2008; Castro, 2010; IMARPE, 2015). This report describes the first record of multiple abnormalities in an embryo of P. glauca collected on the Peruvian coast.
In September 1995, a pregnant P. glauca female was caught product of artisanal fishery in Puerto Nuevo, Piura, Peru (27°06'23”W, 05°05'28”S) with an unusual embryo with multiple abnormalities in the region of the head and trunk. The information about weight and the total length of the female blue shark could not be obtained. The embryo was preserved in a 10% formaldehyde solution, which later was changed to 70% ethylic alcohol and stored in the Ichthyologic Scientific Collection from the Peruvian Marine Research Institute with catalog number: IMARPE 01-000148. For species identification, we reviewed studies of Chirichigno & Vélez (1998) and Romero et al. (2015). The specimen was measured, photographed and radiographed using Examion CR Vita 25 equipment.
The anomalous embryo was a female P. glauca with a total length of 25.2 cm and weight of 104.27 g. The embryo presented head with a pair of nostrils with two dorsal and pectoral fins, one anal fin, and one caudal fin. However, in the cephalic region, duplicated structures were observed: two mouths opened laterally, converging in a common pharyngeal duct and three ocular sockets that could correspond to the eyes (Fig. 1). The embryo showed an axial skeleton with thoracic lordosis, defines by an exaggerated curvature of the vertebral column in the lumbar area. Likewise, at the posterior end of the trunk was rolled in an anticlockwise direction from pelvic to caudal fin (named “screw-shaped”), as it can be observed in radiograph picture (Fig. 1).
Figure 1 a) Anomalous embryo of the blue shark, Prionace glauca from Puerto Nuevo, Piura, Peru (southeast Pacific) with multiple morphological anomalies, b) ventral view of X-ray plate showing the three eyes (e1, e2 and e3) and two mouths (m1 and m2), c) dorsal view of X-ray plate showing a thoracic lordosis (tl) and dextrorotatory helical (dh).
In southeast Pacific, reports of morphological anomalies in sharks remain rare. Two more cases have been reported, one of them in a P. glauca embryo collected off the Chilean coast (Hevia-Hormazábal et al., 2011) and the other one in a Carcharhinus porosus embryo from Colombian coast (Muñoz-Osorio et al., 2013). Here, we reported the first record of multiple abnormalities in a P. glauca embryo collected off the Peruvian coast. This embryo showed duplicate face parts (mouth and eyes) in a single head, which indicates a morphological anomaly named diprosopia (Biasibetti et al., 2011). The additional middle eye socket could indicate an early diprosopia stage, in which eyes are still developing. In sharks, this anomaly is commonly confused with bicephaly (Sans-Coma et al., 2016). This last is related to conjoined twins with two entirely separated heads on one trunk (Bondeson, 2001). Diprosopia could be the result of several development problems such as duplications parts derived from the branchial arch, complex bifurcation of the notochord, duplications of olfactory placodes, or neural crest (Maisels, 1981; Carles et al., 1995; Sans-Coma et al., 2016).
Furthermore, our specimen showed thoracic lordosis and helical torsion in the trunk area, which has been previously recorded for blue shark (Mancini et al., 2006; Hevia-Hormazábal et al., 2011; Lamarca et al., 2017; Pastén-Marabio et al., 2018). These skeletal abnormalities could be related to parasitic infections, injuries, malnutrition, vitamin C deficiency or congenital diseases (Mahajan & Agrawal, 1979; Wimberger, 1993; Heupel et al., 1999). On the other hand, it is known that morphological abnormalities registered in blue shark may be related to high embryo production (Mancini et al., 2006), varying from 28 to 54 embryos per litter, reaching a maximum record of 135 embryos (Compagno, 1984; Castro et al., 1999). In this species, uterus reduction due to a high number of embryos generates abnormal embryo development (Mancini et al., 2006; Ramírez-Amaro et al., 2019).
Another factor that can be affecting the malformation presence is environmental degradation or pollution (Goto et al., 1981; Ferreira et al., 2002; Rosa et al., 2004; Mancini et al., 2006). In this context, some studies have been reported presence of high levels of heavy metals (e.g., Hg) (Barrera-García et al., 2012; Rodríguez-Romero et al., 2018) and genetic alterations related with initial stages of development (Mancini et al., 2006; Rodríguez-Romero et al., 2018). Although the lack of information about the causes of anomalies, an explanation for some individual reported in this study who did not survive after birth, could be related with difficulties in swimming, feeding and avoiding predators in these individuals (Mancini et al., 2006; Rodríguez-Romero et al., 2018).
Current and previous reports about morphological anomalies shed light on the possible causes of these deformations in sharks (Ramírez-Amaro et al., 2019), but more studies about this topic are needed, especially in commercial relevant species.
