Patrick Lemell

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.

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.

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.

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. J. Morphol., 2011.

Kinematical Analysis of Animal Behaviour: The Challenge to Increase the Frame Rate in Digital High-Speed Cinematography

ABSTRACT Modern digital high-speed film systems are able to capture sequences by extremely high frame rates—over 100 000 fr/s. The equipment costs for such systems are high but the operational costs are practically zero. An important advantage of digital versus analogue high-speed films is the possibility to automatically “digitize” defined markers. The contrast and brightness of the sequences can be modulated in wide ranges; even at very high frame rates, a film can therefore be shot at relatively low light intensity. The construction and sensitivity of modern charge-coupled device (CCD) detectors allow filming with relatively high resolution at over 10 000 fr/s. The only remaining limiting factor for increasing the frame rate is the light level to which the animals are tolerant and still behave “normally” during the experiments. The present study uses film sequences from feeding events and defensive responses in animals, but also films of pistol shots, to demonstrate that choosing an adequate frame rate is crucial for any kinematical analysis.

Size does matter – Intraspecific variation of feeding mechanics in the crested newt Triturus dobrogicus (Kiritzescu, 1903)

Abstract Many studies have yet been conducted on suction feeding in aquatic salamander species. Within the Salamandridae, the crested newt Triturus dobrogicus (Kiritzescu, 1903), occurring from the Austrian Danube floodplains to the Danube Delta, was not subject of investigations so far. The present study examines the kinematics of aquatic suction feeding in this species by means of high-speed videography. Recordings of five individuals of different size and sex while feeding on bloodworms were conducted, in order to identify potential discrepancies among individuals and sizes. Five coordinate points were digitized from recordings of prey capture and twelve time- and velocity-determined variables were evaluated. All specimens follow a typical inertial suction feeding process, where rapid hyoid depression expands the buccal cavity. Generated negative pressure within the buccal cavity causes influx of water along with the prey item into the mouth. Results demonstrate higher distance values and angles for gape in individuals with smaller size. In addition, hyoid depression is maximized in smaller individuals. While Triturus dobrogicus resembles a typical inertial suction feeder in its functional morphology, intraspecific differences could be found regarding the correlation of different feeding patterns and body size.