Teratological records in blue shark Prionace glauca embryos from the South-western Atlantic Ocean

Abstract

Abnormal embryonic development may result from mutations caused by genetics, environmental conditions or viruses. This study reports cases of cyclopia and a mouth malformation in two embryonic blue shark Prionace glauca collected off southern Brazil (South-western Atlantic). Such malformations are likely to reduce the chances of survival of embryos and neonates.

Introduction

Within the last two decades, reports of abnormalities in elasmobranch embryos have increased worldwide, and a wide variety of abnormal morphological conditions have been described. The reports come from a range of seas and oceans, including the Atlantic Ocean (Clark, 2002; Coelho & Erzini, 2006; Mancini et al., 2006; Delpiani et al., 2011; Zaera & Johnsen, 2011; Wagner et al., 2013; Dos Santos & Gadig, 2014; Afonso et al., 2016; Lamarca et al., 2017; Ramírez-Amaro et al., 2019; Prado et al., 2020), Pacific Ocean (Goto et al., 1981; Clark, 2002; Bejarano-Álvarez et al., 2011; Galván-Magaña et al., 2011; Hevia-Hormazábal et al., 2011; Bejarano-Álvarez & Galvãn-Magaña, 2013; Muñoz-Osorio, et al., 2013; Escobar-Sanchez et al., 2014; Becerril-García et al., 2017; Pastén-Marambio et al., 2018; Rodriguez-Romero et al., 2019), Mediterranean Sea (Saidi et al., 2006; Bottaro et al., 2008; Sans-Coma et al., 2016), Caribbean (Ehemann et al., 2016) and Indian Ocean (Moore, 2015).

The most frequently reported abnormalities are related to the anterior body region, such as: dicephaly (Galván-Magaña et al., 2011; Rodriguez-Romero et al., 2019), cyclopia (Bejarano-Álvarez & Galván-Magaña, 2013; Ramírez-Amaro et al., 2019) and duplicate or absent structures (e.g. two mouths, Mancini et al., 2006; missing gill slits, Saidi et al., 2006). Furthermore, trunk abnormalities (e.g. spinal anomalies, Parenzan, 1979; Lamarca et al., 2017; Kanagasuku et al., 2020) and albinism (Escobar-Sanchéz et al., 2014; Becerril-García et al., 2017) have also been reported.

Blue shark Prionace glauca (Linnaeus, 1758) is the most abundant oceanic shark and represents an important fishery resource (Clarke et al., 2014; Gilman et al., 2016), especially in Brazil (Barreto et al., 2017). This highlights the need of reporting abnormalities in an effort to elucidate the frequency of events of this nature. Additionally, the wide distribution and life-history characteristics of P. glauca, which includes placentotrophy, a gestation period of 9–12 months, litter size of 4–63 individuals (exceptionally up to 135 embryos) (Balon, 1975; Compagno, 1984; Dulvy & Reynolds, 1997; Compagno & Niem, 1998) and size at birth (35–44 cm total length; Compagno, 1984), makes P. glauca an important model organism to improve our knowledge about the causes and morphological consequences of embryonic abnormalities in viviparous elasmobranchs. This paper reports two different cases of abnormal development in P. glauca embryos, both collected from Southern Brazilian waters.

Methods

Two pregnant blue shark females were caught off the coast of Rio Grande do Sul, Brazil during commercial surface longline activities. The first specimen was caught on 7 September 2018 (32°50′S 50°05′W) by the fishing vessel ‘Sambaqui III’, and the abnormal embryo (embryo A) was extracted from the uterus during attempts to release the pups alive. The second specimen was caught on 16 November 2019 (35°27′S 49°04′W) by the fishing vessel ‘Áustria’. This individual (197 cm fork length) was examined by a scientific observer and one embryo in a litter of 27 pups displayed abnormal development (embryo B). Both embryos were transferred to the Demersal Resources and Cephalopods Laboratory of Oceanography Institute of Federal University of Rio Grande (FURG).

The abnormalities of both embryos were described based on a morphological perspective. Subsequently, the embryos were fixed in formaldehyde and deposited in the collection of the FURG.

Results

Embryo A (voucher specimen code CC00321) showed synophthalmia, a type of cyclopia (Torczynski et al., 1977) and its caudal fin severely coiled anticlockwise (Figure 1A). This specimen showed a malformation in the rostrum by a deficient development of the chondrocranium. Spiracles were present, as well as five gill slits, however, nostrils were absent (Figure 1B). The two-eye-fusion was displaced ventrally, on a large single orbital cavity, possibly related to a malformation in the basitrabecular process. The mouth was normally developed and showed a well-built adductor mandibular complex (i.e. quadratomandibularis and preorbitalis muscles) and intermandibularis muscle (Figure 1C). The posterior region of the body, from the second dorsal fin onward, had coiled in an anticlockwise direction (Figure 1D).

Fig. 1. Prionace glauca embryo A: (A) dorsal view exhibiting the trunk and chondrocranium malformations, (B) lateral view showing spiracles and gill slits, (C) ventral view displaying the synophthalmic eye and the mouth, and (D) rolled ‘anticlockwise’ body posterior part.

Embryo B (voucher specimen code CC00322) presented an incomplete fusion at the right corner of the mouth that can be viewed ventrally and from a lateral angle. In dorsal view, a slight misalignment in the location of the eyes is observed (Figure 2A), but apart from that, the individual did not present other obvious visual deformations (Figure 2B). The ventral view of the anterior body end of embryo B compared with one of its siblings shows the difference in the position of the eyes of embryo B (Figure 2C). The lack of fusion in the right corner of the mouth (Figure 2D) suggests a lack of fusion in this region between the Meckel's cartilage and the palatoquadrate, that in turn generated a malformation in the right dorsal and ventral quadratomandibularis muscles and a displacement in the structures of the chondrocranium, causing misalignment in the orbits.

Fig. 2. Prionace glauca embryo B: (A) dorsal view (upper: embryo B; lower: sibling), (B) lateral diagonal view displaying the malformation in the mouth (upper: embryo B; lower: sibling), (C) ventral view comparing with its sibling (left: sibling; right: embryo B), and (D) zoom to the malformed mouth.

Discussion

According to the classification of morphological anomalies by Hennekam et al. (2013), embryo A presents a major morphology anomaly because it has significant consequences on its health and appearance at the time of evaluation, whilst embryo B has a minor morphological anomaly since there is a low impact on appearance with minimal health consequences.

Even though embryonic development was still in progress, the survival chance after birth would likely be small due to swimming disabilities for embryo A and feeding difficulties for both specimens.

Abnormalities related to cyclopia have been reported before for embryos of other elasmobranch species such as Carcharhinus obscurus (Bejarano-Álvarez & Galván Magaña, 2013), Galeorhinus galeus (Ramírez-Amaro et al., 2019) and Squatina californica (synophthalmia; Escobar-Sánchez et al., 2014), while specific mouth malformations have not been reported for elasmobranchs.

As shown in Table 1, malformations in P. glauca embryos have been widely reported in different marine regions. However, similar reports in the South Atlantic Ocean are less frequent in comparison with the North Atlantic Ocean. In both the Atlantic and Pacific Oceans, the most commonly reported malformations for this species at this stage of development are diprosopia (usually two heads) and twisted vertebral columns (Mancini et al., 2006; Bejarano-Álvarez et al., 2011; Galván-Magaña et al., 2011; Hevia-Hormazábal et al., 2011; Ehemann et al., 2016; Lamarca et al., 2017; Pastén-Marambio et al., 2018; Rodriguez-Romero et al., 2019; Ramírez-Amaro et al., 2019; Kanagusuku et al., 2020). In this study, we report the second embryo with a kind of cyclopia for the South-western Atlantic Ocean (Ferreira et al., 2002).

Table 1. Morphological abnormalities reported in Prionace glauca embryos worldwide

The abnormalities observed in blue sharks and their relatively frequent occurrence could be explained by their high production of embryos, with a maximum litter size of 135 (Smith, 1997). The causes for embryonic abnormalities could include the effects of contaminants (Casarini et al., 1997; Rosa et al., 2004), as elasmobranchs are particularly vulnerable to bioaccumulation and biomagnification of pollutants due to their longevity and high trophic level (Gelsleichter & Walker, 2010). Moreover, abnormalities such as spinal malformations could be caused by arthritis, injuries, parasites, poor nutrition or tumours (Sadowsky, 1971; Schwartz, 1973; Heupel et al., 1999). Theoretically, if population declines resulted in higher levels of inbreeding, this might also increase the likelihood of malformations in embryonic development (Dulvy et al., 2014; Lamarca et al., 2017).

The number of developmental abnormalities reported in sharks has increased over time, although it is uncertain as to whether this relates to anthropogenic impacts or simply an increase in sampling and reporting. More standardized sampling and reporting of embryos would be required to inform on this. Despite the difficulty in making assumptions about possible causes for embryonic abnormalities, reporting of morphological abnormalities needs to be encouraged because it will allow us to better understand their causes, if there are species with a greater predisposition to these malformations, or even to understand the juvenile survival rate, which is an essential parameter for stock assessment.