Investigations into the morphometrics, uterine tissue adaptation, maternal fluid biochemistry, heavy metal offloading and early embryonic teeth development impacting the reproductive strategy of the female Ragged-tooth shark (Carcharias taurus)

Abstract

Vulnerable” status of ragged-tooth sharks (Carcharias taurus) in South Africa caused by overexploitation, late maturity and low fecundity suggests an intervention to increase the size of this population is needed. Achieving this will require an understanding of all aspects linked to this species maternal-embryonic relationship.

Morphometric relationships, uterine histology and maternal fluid biochemistry were 8 assessed in C. taurus through all the respective reproductive stages (RS) from non-gravid (immature to mature-sexually active; RS1-3) to gravid (i.e. only capsules found; RS4 or capsules and pups found; RS5A-5E) females. Examination of metals in the maternal fluids and embryonic dentition were only examined in early-staged gravid females (i.e. RS5A).

Haematoxylin/Eosin and Periodic Acid Schiff-Alcian Blue stains in conjunction with light microscopy was used to assess the uterine epithelium and wall while scanning electron microscopy further evaluated the epithelium. These techniques revealed an increase of the uterine lamellae (folds) protruding into the lumen lined with micro-ridges containing blood vessels. The close proximity of blood vessels to the lumen filled with uterine fluid and the decrease in wall thickness as pregnancy progressed suggests an adaption for the exchange of respiration and osmoregulation in the developing aplacental embryos. Although there is no evidence for uterine secretion through structural adaptations, the female supports the embryos nutritional requirement through embryonic tissue (intrauterine cannibalism) and yolk (oophagy) provisions. The pivotal interplay of the liver and ovary, during vitellogenesis, that impact on yolk formation was evident during the morphometric evaluation of hepatosomatic and gonadosomatic indices. Length, weight, uterine width, capsule production and migration trends of the females as well as length and weight relationship of the embryos were tabulated.

Reproductive hormones, assessed in maternal fluids (i.e. plasma (in RS1-5D females), uterine fluid (in RS4-5D females) and intracapsular fluid (in RS5A females), showed that follicle-stimulating-, progesterone- and oestradiol hormones were responsible for promoting vitellogenesis and encapsulation which led to three main stages where the rate of ovulation increases in the female. Clinical biochemistry analysers confirmed the composition and concentration of biochemical analytes in same maternal fluids, which were found to be higher in the plasma.

Finally, heavy metals were found to be present in all three fluids, but found highest in the plasma, using inductively coupled mass spectrophotometry. In addition, variable pressure (VP) SEM confirmed the dental composition of the embryonic teeth found in the jaws of some embryos that appeared to escape encapsulation earlier than previously documented. It would appear that the embryos are creating adaptive ways to survive the intracannibalistic stage (RS5C) by escaping encapsulation early. However, the presence of heavy metals in the maternal fluids that surround the embryos could compromise their development over time; creating concern for a species that is Vulnerable.

This study, which serves as the first detailed analysis of the maternal-embryonic relationship, may serve as areas to model in forthcoming programmes aimed at increasing the numbers of this species.