Josef Weisgram

Morphology and Function of the Feeding Apparatus of Pelusios castaneus (Chelonia; Pleurodira)

ABSTRACT Feeding mechanics of vertebrates depend on physical constraints of the surrounding media, water or air. Such functions are inseparably combined with form. The aim of this study is to show this linkage for the pleurodiran freshwater turtle Pelusios castaneus and, additionally, to point out the major functional and biomechanical distinctions between aquatic and terrestrial feeding turtles as well as several intermediate forms. Gross morphological investigations of skull, hyoid, tongue, and connected musculature, as well as scanning electron microscopy of the tongue surface, show typical features of an aquatic feeder, e.g., strongly developed hyoid apparatus vs. a small tongue with only moderate papillae, and massive jaw and hyoid musculature. Additionally, the special function of the esophagus during feeding is investigated to elucidate the problems of a bidirectional feeder. The esophagus is highly distensible in order to store the excess water sucked in during feeding until the prey is fixed by the jaws. The distension is probably achieved by a coincidence of active (branchial horn) as well as passive (water) components. P. castaneus is a feeding generalist, and is well adapted to the aquatic medium in terms of its functional as well as morphological features. J. Morphol. 244:127–135, 2000.

Fine structure of the dorsal lingual epithelium of Trachemys scripta elegans (Chelonia: Emydidae)

Turtles are adapted to different environments, such as freshwater, marine, and terrestrial habitats. Examination of histological and ultrastructural features of the dorsal lingual epithelium of the red‐eared turtle, Trachemys scripta elegans, and comparison of the results with those of other turtles should elucidate the relationship between the morphology of tongues as well as the fine structure of lingual epithelia and chelonian feeding mechanisms.

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. J. Morphol., 2009.

FEEDING MECHANISM OF TESTUDO HERMANNI BOETTGERI (CHELONIA, CRYPTODIRA)

Feeding of Testudo hermanni boettgeri was studied by film analysis and anatomical examination of the musculature and skeleton elements involved. Film sequences were analysed to describe the movements of food item, neck, jaws, and tongue. The feeding cycle is divided into food uptake (ingestion), followed by several transport and manipulation cycles (intraoral transport), and finally swallowing of the food (deglutition). The results show that in Testudo hermanni boettgeri the tongue is the main tool for food uptake and intraoral manipulation. The hyoid apparatus supports the floor of the mouth and is adapted to the highly movable tongue. Compared to aquatic species the hyoid is smaller, more flexible, and less ossified. Skull shape and arrangement of jaw muscles also demonstrate adaptation to terrestrial life. The jaw muscles are less developed, their insertion areas are smaller and do not extend as much caudally as in aquatic species. The organisation of the feeding mechanism in tetrapods depends on biophysical constraints imposed by the surrounding medium. In this organisation the hyolingual complex plays an important role. The tongue of terrestrial turtles tends to be larger, more muscular, more mobile, and tends to have a more complex surface than in aquatic forms. The feeding mechanism of Testudo hermanni boettgeri shows the typical situation of a turtle that is fully adjusted to terrestrial life.

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.

Feeding Patterns of Pelusios Castaneus (Chelonia: Pleurodira)

The aim of this study is to describe the feeding patterns of the pleurodiran West African mud turtle Pelusios castaneus. The kinematics of feeding were studied for two types of prey (fish, snail) to provide a description of the feeding cycle and to determine whether kinematic patterns can be altered in response to prey size and type. High-speed film recordings (250 frames/s) of feeding cycles were evaluated. Five variables were measured and four velocities were calculated. The feeding cycle was divided into five phases: preliminar head fixation, final head fixation, final head approach, grasp followed by manipulation and a transport phase, and suction end position which is followed by swallowing. The turtle has the ability to modulate the feeding kinematics depending on prey type. Furthermore, two types of suction were distinguished, compensatory suction and inertial suction. While compensatory suction is used mainly for prey capture, inertial suction is needed during the manipulation and transport phase, and becomes more important the longer these phases last. A Ram-Suction-Index was used to show the relation between the ram and the suction component during the different phases of the feeding cycle. The results show that the smaller and less agile the prey, the more the turtles enhance the suction component of their feeding patterns. Hydrodynamically induced kinematic similarities in aquatic feeding of fish, larval aquatic salamanders and turtles were found, as well as differences that result from the fundamentally different morphological design of the feeding apparatus.

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.

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. Anat Rec, 291:876‐885, 2008.

The feeding apparatus of Chelus fimbriatus (Pleurodira; Chelidae) - adaptation perfected?

The feeding apparatus of the fringed turtle Chelus fimbriatus (Schneider, 1783) was studied to elucidate the feeding mechanics of an aquatic feeding specialist that has never been investigated in detail before, regarding gross morphology. The skull and hyoid apparatus as well as associated musculature were examined by computer tomography and dissection; the tongue was examined by scanning electron microscopy. The flat skull, the possibility to enormously depress the mandible combined with a cheek-like development, the large, ossified hyoid apparatus, and a well-distensible esophagus enable the turtle to produce an enormous suction force the prey is inhaled with. The jaw adductors are poorly developed in relation to other turtles and thus help keep the skull shape flat; nevertheless, they are able to generate high velocities and exhibit some new performance lines. The hyoid musculature is as well-developed as the hyoid apparatus itself, promoting the high depression velocity that is necessary for good feeding performance. The tongue is nearly reduced and lacks dorsal morphological differentiations. Taking all the morphological features into account, C. fimbriatus is an extremely well-adapted turtle making this species a very interesting object of investigation.

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. Anat Rec 293:1416–1424, 2010.