Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue.

In tetrapods, the ability to ingest food on land is based on certain morphological features of the oropharynx in general and the feeding apparatus in particular. Recent paleoecological studies imply that terrestrial feeding has evolved secondarily in turtles, so they had to meet the morphological oropharyngeal requirements independently to other amniotes. This study is designed to improve our limited knowledge about the oropharyngeal morphology of tortoises by analyzing in detail the oropharynx in Manouria emys emys. Special emphasis is placed on the form and function of the tongue. Even if Manouria is considered a basal member of the only terrestrial turtle clade and was hypothesized to have retained some features reflecting an aquatic ancestry, Manouria shows oropharyngeal characteristics found in more derived testudinids. Accordingly, the oropharyngeal cavity in Manouria is richly structured and the glands are large and complexly organized. The tongue is large and fleshy and bears numerous slender papillae lacking lingual muscles. The hyolingual skeleton is mainly cartilaginous, and the enlarged anterior elements support the tongue and provide insertion sides for the well-developed lingual muscles, which show striking differences to other reptiles. We conclude that the oropharyngeal design in Manouria differs clearly from semiaquatic and aquatic turtles, as well as from other reptilian sauropsids.

The fish in the turtle: on the functionality of the oropharynx in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae) concerning feeding and underwater respiration.

In tetrapods, the oropharyngeal cavity and its anatomical structures are mainly, but not exclusively, responsible for the uptake and intraoral transport of food. In this study, we provide structural evidence for a second function of the oropharynx in the North American common musk turtle, Sternotherus odoratus, Kinosternidae: aquatic gas exchange. Using high-speed video, we demonstrate that S. odoratus can grasp food on land by its jaws, but is afterward incapable of lingual based intraoral transport; food is always lost during such an attempt. Scanning electron microscopy and light microscopy reveal that the reason for this is a poorly developed tongue. Although small, the tongue bears a variety of lobe-like papillae, which might be misinterpreted as an adaptation for terrestrial food uptake. Similar papillae also cover most of the oropharynx. They are highly vascularized as shown by light microscopy and may play an important role in aquatic gas exchange. The vascularization of the oropharyngeal papillae in S. odoratus is then compared with that in Emys orbicularis, an aquatic emydid with similar ecology but lacking the ability of underwater respiration. Oropharyngeal papillae responsible for aquatic respiration are also found in soft-shelled turtles (Trionychidae), the putative sister group of the kinosternids. This trait could therefore represent a shared, ancestral character of both groups involving advantages in the aquatic environment they inhabit.

Three types of cutaneous glands in the skin of the salamandrid Pleurodeles waltl. A histological and ultrastructural study.

Histological and ultrastructural investigations revealed three different multicellular skin gland types in the salamandrid Pleurodeles waltl. The mucous glands are small, with one layer of secretory cells surrounding a central lumen; they produce the viscous and slippery mucus film that has various functions in amphibians. The serous glands can be divided based on their histological and ultrastructural characters into the granular gland Type I (GGI) and the granular gland Type II (GGII). The first type (GGI) is moderately sized and distributed throughout the body surface, with higher concentrations in the parotoid and back regions. In contrast, the second type (GGII) is very large (for Pleurodeles) and was found only in the tail, with highest concentration in the tail dorsum. Both granular gland types contain mainly proteinaceous materials but differ in their morphological features including size, shape, cellular organization and vesicle distribution, vesicle size and vesicle shape. Both GGI and GGII are especially concentrated in body parts that are presented to an attacking predator and are hypothesized to produce repellent to poisonous substances to thwart potential aggressors.

Analysis of prey capture and food transport kinematics in two Asian box turtles, Cuora amboinensis and Cuora flavomarginata (Chelonia, Geoemydidae), with emphasis on terrestrial feeding patterns.

This study examines the kinematics and morphology of the feeding apparatus of two geoemydid chelonians, the Malayan (Amboina) box turtle (Cuora amboinensis) and the yellow-margined box turtle (Cuora flavomarginata). Both species are able to feed on land as well as in water. Feeding patterns were analysed by high-speed cinematography. The main focus of the present study is on the terrestrial feeding strategies in both Asian box turtles, because feeding on land has probably evolved de novo within the ancestrally aquatic genus Cuora. During terrestrial feeding (analysed for both species), the initial food prehension is always done by the jaws, whereas intraoral food transport and pharyngeal packing actions are tongue-based. The food uptake modes in Cuoras differ considerably from those described for purely terrestrial turtles. Lingual food prehension is typical of all tortoises (Testudinidae), but is absent in C. amboinensis and C. flavomarginata. A previous study on Terrapene carolina shows that this emydid turtle protrudes the tongue during ingestion on land, but that the first contact with the food item occurs by the jaws. Both Asian box turtles investigated here have highly movable, fleshy tongues; nonetheless, the hyolingual complex remains permanently retracted during initial prey capture. In aquatic feeding (analysed for C. amboinensis only), the prey is captured by a fast forward strike of the head (ram feeding). As opposed to ingestion on land, in the underwater grasp the hyoid protracts prior to jaw opening. The head morphology of the investigated species differs. In contrast to the Malayan box turtle, C. flavomarginata exhibits a more complexly structured dorsal lingual epithelium, a considerable palatal vault, weaker jaw adductor muscles and a simplified trochlear complex. The differences in the hyolingual morphology reflect the kinematic patterns of the terrestrial feeding transport.

Microanatomy of the palatal mucosa of the semiaquatic malayan box turtle, Cuora amboinensis, and functional implications.

Scanning Electron Microscopy (SEM) revealed that the palate of Cuora amboinensis has a flat surface with keratinized and non-keratinized regions. Keratinization is reflected in disc-shaped keratinized dead cells with rough microplicae on the surface, and is concentrated close to the rhamphotheca. The surface of the non-keratinized hexagonal epithelial cells is dotted with microvilli and sometimes with cilia. Taste buds are present both in lightly keratinized and non-keratinized regions and exhibit a crater-like shape. Light microscopy shows the different tissue layers of the oral mucosa and the different epithelial structures. In keratinized regions, keratinocytes mature from basal to superficial, where they build up keratin layers of varying thickness. In non-keratinized regions, the epithelial cells are arranged in a stratified fashion, and cuboidal to cylindric cells form a superficial layer. Goblet cells appear to be diffusely distributed, but are often organized in goblet cell fields which can be folded into crypts. Taste buds consist of slender epithelial cells, exhibit the typical barrel-like shape and are specially concentrated in the anterior, praechoanal palate. This anterior concentration of taste buds is shown by kinematographic analysis to correlate with the food prehension mode in Cuora amboinensis. The lamina propria of the palatal mucosa consists of loose connective tissue with inflammatory cells between capillaries. All these structures of the oral mucosa act as a functional entity and help determine how successfully an organism adapts ecologically to the environment.

The dorsal lingual epithelium of Rhinoclemmys pulcherrima incisa (Chelonia, Cryptodira).

This study employed light microscopic (LM), scanning electron microscopic (SEM), and transmission electron microscopic (TEM) methods to provide detailed morphological information on the histological and ultrastructural features of the dorsal tongue epithelium of Rhinoclemmys pulcherrima incisa. SEM revealed columnar papillae laterally, as well as papillae, which tend to have a ridge-like appearance in the center of the tongue. LM and TEM showed three different zones of lingual epithelium: a stratified apical area with serous cells at the top of the papillae, a stratified lateral area with both serous and mucus cells, and an unstratified glandular area consisting of distinct glandular ducts with mucus cells. Comparison with morphological data from other turtles shows that the lingual epithelial structure in R. p. incisa is in accordance with that observed for other generalized omnivores which prefer a terrestrial lifestyle, thus matching the ecological information about this species.

Feeding patterns of Chelus fimbriatus (Pleurodira: Chelidae).

The kinematics of feeding on fish have been studied in the aquatic feeding specialist Chelus fimbriatus, the fringed turtle, to provide a basic description of complete feeding cycles. Anatomical findings supplement the kinematic results. High-speed video (500 frames x s(-1)) recordings and X-ray film (150 frames x s(-1)) are used to analyse the kinematic variables characterizing head, hyoid, oesophageal and prey movements. The high velocities, especially of mouth opening, the forward thrust of the head and suction of the prey, are unique among turtles and comparable with those of aquatic salamanders and certain fishes (unidirectional feeders, in contrast to Chelus fimbriatus). The expandability of the pharynx and the anterior half of the oesophagus enables a specific type of unidirectional flow, at least during the early stages of the feeding cycle. This considerably improves the feeding performance compared with that of other aquatic turtles. The streamlined shape of the skull, the large hyoid apparatus, the highly reduced tongue and the extremely distensible oesophagus support the kinematics to a great extent, making C. fimbriatus a specialized suction feeder that can be regarded as one endpoint in the feeding evolution of aquatic reptiles.

Dorsal lingual epithelium of Platemys pallidipectoris (Pleurodira, Chelidae).

Scanning electron microscopy reveals that the flat tongue of Platemys pallidipectoris has shallow grooves and no lingual papillae. The surface of the tongue is covered with dome-shaped bulges, each corresponding to a single cell. Short microvilli are distributed over the cell surface. Light microscopy shows a stratified cuboidal epithelium with an underlying strong connective tissue. Transmission electron microscopy indicates four layers. The basal cells of the epithelium are electron-translucent and have a large central nucleus and a cytoplasm with keratin tonofilaments. Plasma cells with abundant rough endoplasmic reticulum and mitochondria occur in the basal layer. Production of secretory granules begins in the more electron-dense intermediate layers and increases as the cells move toward the surface. The membranes of the cells of the deep intermediate layer form processes that project into relatively wide intercellular spaces. In the superficial intermediate layer, the cytoplasm of the cells contains numerous fine granules; these increase in number but not in size in more distal layers. The cells of the surface layer are electron-translucent with a round nucleus. Contents of their fine granules are secreted into the oral cavity. © 1995 Wiley-Liss, Inc.