Congenital Craniofacial Abnormalities in Olive Ridley Sea Turtle Hatchlings

Abstract

The Olive Ridley (Lepidochelys olivacea), is the most abundant species of sea turtles in the world, but is still threatened according to the red list of endangered species. Apparently, the Olive Ridley turtle seems more prone to congenital malformations compared to other species of sea turtles. In northwestern Mexico, an incidence of congenital malformations of 2% has been reported for this species, most of which occur in the craniofacial region (49%). The objective of this study was to deduce the etiology of the malformations based on the pattern of the affected structures. During the 2019 nesting season at El Caimanero nesting beach, Sinaloa, Mexico, 11 specimens with external craniofacial malformations and 10 that did not show external malformation were collected. The normal animals hatched, but died from other natural causes within the nests. Specimens were divided between histological analysis or µCT with phosphotungstic acid contrast enhancement. Specimens with malformations consistent with a Holoprosencephaly (HPE) phenotype were detected (Table 1). Analysis PTA staining and µCT showed there was a single external naris. There was variability in the morphology of the nasal passages. Other midline structures were also deficient including absent interorbital septum and small premaxilla. However, two other cardinal signs of severe HPE were not seen. The brain was divided into right and left hemispheres and the eyes were separated. There were additional defects in the mandible affecting mesodermal derivatives of the first arch. The tongue was severely hypoplastic and the musculature in the floor of the oral cavity was deficient. The tracheal opening was also displaced posteriorly in the tongue compared to the usual position in the center of the tongue. The nasal defects may be caused by a hypoplastic frontonasal process which allows merging of the nasal pits. The muscular deficiencies in the tongue are likely due to incomplete formation of lingual swellings in the first pharyngeal arch. Nasal development was normal in the majority of animals and the most common defect was mandibular deviation combined with hypoplasia. The defects observed are consistent with a mild form of HPE but also with ciliopathies that include tongue agenesis. Further histological analysis will be carried out to assess cellular and molecular phenotypes. This work suggest pleotropic environmental effects cause the embryonic defects after the eggs are oviposited in the nest. This turtle species lays eggs with embryos in the gastrula stage of development, reaching pharyngula stage, 3-4 days after laying. Therefore, we postulate an exposure to an environmental teratogen in the first 4 days is responsible for the congenital abnormalities.