Dr. Christian Beisser

Address:
Department of Theoretical Biology,
Morphology Section
University of Vienna
Althanstraße 14
A - 1090 Vienna
Austria, Europe

Phone: *43-1-4277-544 14
Fax: *43-1-4277-9544
Email:

Homepage:
http://homepage.univie.ac.at/christian.beisser/

der administrator

From November 1998 to December 2001, I was research assistant at my department, working for the 'turtle project'. Within this project, I was busy with electron microscopy:
Scanning electron microscopy was used to show the surface topography of tongue and esophagus in the studied species adapted to water in a different extent. At higher magnification, surface structures of single cells were studied in order to investigate if differences between the species can be found.
Light microscopy and transmission electron microscopy of lingual and esophagial epithelium after standard fixation methods allowed the description of different cell types within the single cell layers. The usage of modified staining methods enhanced the visualization of connective tissue fibres, structures of the basement membrane and intermediate filaments, or gave enhanced membrane contrast as well as selective staining of structures containing carbohydrates.
Right now, I am still working on lingual eithelia of turtles finishing the project's work, as well as examining new species ...

Prof. Dr. E. Mayrhofer (A); University of Veterinary Medicine, Vienna; Clinic of Radiology

Beisser, CJ., Weisgram, J. & H. Splechtna (1995)
The dorsal lingual epithelium of Platemys pallidipectoris (Pleurodira, Chelidae).
Journal of Morphology 226: 267-276. [Abstract + Reprint request]

Beisser, CJ., Weisgram, J., Hilgers, H. & H. Splechtna† (1998)
Fine structure of the dorsal lingual epithelium of Trachemys scripta elegans (Chelonia: Emydidae).
The Anatomical Record 250: 127-135. [Abstract + Reprint request]

Nussbaumer, AD., Bright, M., Beisser, CJ. & JA. Ott (2000)
Biochemical characterisation of the recognition/maintenance mechanism between thiotrophic ectosymbionts and Stilbonematinae.
In: H. Chr. Weber, S. Imhof and D. Zeuske. Programs, Abstracts and Papers of the Third International Congress on Symbiosis. Philipps University of Marburg, Germany, p 159.
[ contact: andrea.nussbaumer@univie.ac.at c/o Dept. Marine Biology ]

Nussbaumer, AD., Bright, M., Beisser, CJ. & JA. Ott (2001)
Partner recognition and maintenace in a highly specific association between ectosymbiotic bacteria and marine nematodes.
In: Abstract Book of the Eleventh International Meiofauna Conference (ELIMCO). Boston University University, Boston, Massacusetts, p 46.
[ contact: andrea.nussbaumer@univie.ac.at c/o Dept. Marine Biology ]

Nussbaumer, AD., Bright, M., Baranyi, C., Beisser, CJ. & JA. Ott (2004)
Attachment mechanism in a highly specific association between ectosymbiotic bacteria and marine nematodes.
Aquatic Microbial Ecology 34: 239–246.
[ contact: andrea.nussbaumer@univie.ac.at c/o Dept. Marine Biology ]

Wagner, FH. & CJ. Beisser (2005)
Does carbon enrichment affect hyporheic invertebrates in a gravel stream?
Hydrobiologia 544: 189-200.
[ contact: franz.wagner@baw.at ]

Ladich, F. (2001)
Sound-Generating and -Detecting Motor System in Catfish: Design of Swimbladder Muscles in Doradids and Pimelodids.
The Anatomical Record 263: 297-306.
[ contact: friedrich.ladich@univie.ac.at c/o Uni Vienna ]

Ladich, F. & AN. Popper (2001)
Comparison of the inner ear ultrastructure between teleost fishes using different channels for communication.
Hearing Research 154: 62-72.
[ contact: friedrich.ladich@univie.ac.at c/o Uni Vienna ]

Beisser, CJ., Weisgram, J. & H. Splechtna (1995)
The dorsal lingual epithelium of Platemys pallidipectoris (Pleurodira, Chelidae).
Journal of Morphology 226: 267-276.

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, 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.

Background: 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 morphology of tongues as well as fine structure of lingual epithelia and chelonian feeding mechanisms.
Methods: Light microscopical (LM), scanning (SEM) and transmission (TEM) electron microscopical methods were used.
Results: SEM revealed a distribution of lingual papillae all over the dorsal tongue surface. Single epithelial cells can be discerned, with short microvilli on their surface. LM studies show differences within the stratified epithelium between the lateral and the apical side of the papillae. In TEM, these differences become more obvious: while the basal and deep intermediate layer is similar in both sides of the papillae, mucus granules begin to form at the edge of the superficial intermediate layer at the lateral side. Cells containing fine secretory granules are visible there, too. On the other hand, at the apical side, only fine-granule-containing cells are visible.
Conclusions: This study indicates, that the histology and ultrastructure of the lingual epithelium of Trachemys scripta elegans is similar to that of other turtles adapted to freshwater environments, but differs from turtles living in marine or terrestrial habits. These differences can be explained in terms of the adaptation of turtles to their particular life circumstances.

Summary of my diploma thesis:
Using light and electron microscopic methods, the epithelium covering the dorsal side of the tongue in two chelonian species was observed. Subjects of the examination have been Platemys pallidipectoris Freiberg 1945 and Trachemys scripta (Schoepf, 1792) elegans (Wied, 1839), two species adepted to life in an aquatic environment in a different extent.
Between the two species differences in the dorsal tongue morphology are present. The surface of the tongue of P. pallidipectoris is almost flat; on the contrary, on the tongue of T. s. elegans papillae are clearly formed. This is in agreement with other findings which are found out to date concerning the different feeding mechanisms of water living, semi-terrestrial or completely terrestrial living vertebrates: a small tongue is better in species using suction-feeding as main mechanism for feeding. The rush of water, which occurs when the floor of the mouth is suddenly lowered, sucks the food into the oral cavity. The semi-aquatic species T. s. elegans is able to feed on land too, but therefore a more moveable tongue with mucus cells for manipulation and for making slippery of the food is necessary. The microanatomical and ultrastructural structure of the tongue epithelium and its cells is in a general way the same as observed in other vertebrates. Four layers are distinguishable: the basal layer with the basement membrane, the deep intermediate and the superficial layer and the surface layer. In T. s. elegans, one can distinguish between a mainly mucus secreting area on the lateral side of the papillae and an apical area without mucus cells. In P. pallidipectoris, on the other side, only one type of secreting cells is visible in the tongue epithelium.

Beisser, CJ., Lemell, P. & J. Weisgram (1997)
Morphology of the tongue surface of Pelusios castaneus (Chelonia, Pleurodira) with comments on its function.
Journal of Morphology 232: 3; p. 233 (Abstract).
(Poster at the 5. International Congress of Vertebrate Morphology; Bristol, 12. 7. - 17. 7. 1997)

Among turtles, generally two modes of feeding have been recognized: A terrestrial feeding pattern, where the animal uses its tongue for manipulation of food, and an aquatic suction feeding mechanism, where water acts as a hydraulic tongue. Whereas in the terrestrial mode a prominent tongue is useful, in the latter type a small tongue is necessary in order to prevent hindrance of the rush of water into the mouth. In the present study, tissue samples were fixed and afterwards prepared for scanning electron microscopy. The tongue of Pelusios castaneus is somewhat triangular in shape with a round apex. At low magnification, ridge-like and irregularly shaped structures are visible, which seem to correspond to very moderate papillae. At higher magnification, dome shaped bulges are visible. Each of these bulges coincidents with a single cell of the surface layer of the lingual epithelium. Between these cells cell borders are clearly visible and short microvilli are widely distributed on the free surface side of each cell. This discreet morphology of the dorsal tongue surface reflects on the one hand an aquatic feeding pattern, but on the other hand indicates that this species tends to feed on more immobile prey than other pleurodiran species.

Lemell, P., Beisser, CJ. & J. Weisgram (1997)
Feeding patterns of Pelusios castaneus (Chelonia, Pleurodira) with comments on the morphology of its tongue.
Journal of Morphology 232: 3; p. 285 (Abstract).
(Poster at the 5. International Congress of Vertebrate Morphology; Bristol, 12. 7. - 17. 7. 1997)

Aquatic feeding is the primitive mode of prey capture in vertebrates and is therefore of special interest in the study of vertebrate evolution. The existence of many aquatic-feeding turtles provides morphologists with a group of vertebrates that have evolved aquatic feeding convergently with anamniote feeding systems. High-speed film recordings (250 frames/sec.) of feeding cycles of the semiaquatic freshwater turtle Pelusios castaneus demonstrate, that the turtle has the ability to modulate the feeding kinematics depending on prey type (they were fed fishes and snails). Two types of suction were distinguished, compensatory 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. These turtles show a very original feeding pattern. Pelusios castaneus reflects an aquatic carnivore with smooth buccopharyngeal surfaces and poorly developed papillae and intrinsic tongue musculature. The dorsal tongue surface with its ridge-like as well as irregulary shaped structures indicates, that this turtle is specialized to feed on more immobile prey objects than other aquatic turtles with nonpapillose tongues.

Lemell, P., Beisser, CJ. & J. Weisgram (2000).
Morphology and Function of the feeding apparatus of Pelusios castaneus (Chelonia; Pleurodira).
Journal of Morphology 244 (2): 127-135.

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., strong developed hyoid apparatus versus a small tongue with only moderate papillae; 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.

Beisser, CJ., Lemell, P. & J. Weisgram (2001)
Light and electron microscopy of the tongue of Pelusios castaneus (Chelonia; Pleurodira).
Tissue & Cell 33 (1): 63-71.

The ultrastructure of the dorsal lingual epithelium of the semi-aquatic West African mud turtle, Pelusios castaneus, is described. Our goal is to give additional information to previous studies of this species such as feeding pattern analysis and gross morphology. Tissue specimens were fixed in modified Karnovsky solution followed by osmium tetroxide, embedded in epoxy resin and observed using light and transmission electron microscopy. The dorsal tongue surface is covered with moderate papillae, which are coated by a stratified epithelium overlying a connective tissue core. Two epithelial regions can be differentiated, although differences are not very obvious: the apical area, where granular cells are more abundant than mucus cells, and the lateral area, where cell distribution is opposite. Within the epithelium, different layers are discernable on the basis of the cells’ organelles, corresponding with a process of cell maturation and formation of different granules. These results together with data of previous studies of this species show that the ultrastructure of the lingual epithelium is similar to other turtles adapted to semi-aquatic environments; functional and morphological data indicate a generalist, being well but not highly adapted to feeding in an aquatic environment.

Summary of my Ph.D. thesis:
Using light as well as transmission and scanning electron microscopical methods, the three-dimensional structure of the tongue surface and the composition of the dorsal lingual epithelium of three chelonian species was observed. Subjects of examinations were Chelus fimbriatus, Pelusios castaneus, and Rhinoclemmys pulcherrima incisa, three species adapted to life in aquatic or terrestrial environment to a different extent.
Differences between these three species concern the form of the dorsal tongue morphology as well as the presence of different areas of the epithelium covering the lingual papillae and in the abundance of its two types of secretory cells: in Chelus fimbriatus, the species most adapted to life in water, the tongue is very reduced, and dorsal differentiations are absent. Parts of the lingual epithelium being rich in mucus cells - lingual glands sensu lato - cannot be expected. This has to be interpreted as the best possible adaptation of this carnivorous species to suction feeding, in which a large tongue with lingual papillae would prove to be a hindrance. On the contrary, the generalistic aquatic species Pelusios castaneus shows a functionable tongue with moderate lingual papillae. A differentiation within the dorsal lingual epithelium into an apical area at the oral-sided surface of the papilla and the lateral area at the papilla's lateral sides can be observed; mucus cells are dispersed over the whole lingual epithelium, but concentrate in lateral areas. In a hypothetical sequence of the species observed to date from aquatic to terrestrial, this distribution can be seen as it is the beginning of the formation of lingual glands sensu stricto, and corresponds with the ecology of this omnivorous and aquatic species as well as with its feeding kinematics. Rhinoclemmys pulcherrima incisa, a terrestrial species, has in comparison with similar species a less movable tongue and less prominent lingual papillae at the tongue surface. However, it shows well developed lingual glands in the form of distinct glandular ducts (lingual glands sensu stricto). The preferred habitat land as well as the grasping of the food with the jaws correlates with this morphology.
The ultrastructural composition of the lingual epithelium and its cells fit well into other data from turtles gained to date. Principally, four cell layers have to be distinguished: the basal layer just above the basal membrane, the deep and the superficial intermediate layer, and the surface layer. Deviations from this can be found in parts of the epithelium being rich in mucus cells, where the intermediate layers tend to be reduced or where the stratification is distorted. The process of maturation of both the essential cell types, the granula cells and the mucus cells, and of their secretory granules, is in all observed species comparable and is in agree with data from literature.

Weisgram, J., Beisser, CJ., Lemell, P. & R. Wochesländer (2001)
Aquatic versus terrestrial - which is the primitive turtle feeding mode?
Journal of Morphology 248: 3; p. 299 (Abstract).
(6. International Congress of Vertebrate Morphology; Jena, 21. 7. - 26. 7. 2001)

Present studies on feeding mechanisms show that turtles span the range from fully aquatic to completely terrestrial feeding with many intermediate forms; the question arises which is the basic mode for the whole group. Accepting the theory that turtle-ancestors were terrestrial reptiles means that semi-aquatic and aquatic mechanisms are derived feeding patterns that evolved by reduction of the tongue and strengthening of the hyoid apparatus. The oldest known real turtle is supposed to be an aquatic animal. The lingual feeding mechanism of recent testudinids with their massive and highly movable tongues is a recovery of an ancient feature. However, box-turtles of the Genara Cuora or Terrapene are perfectly adapted to feed on land as well as under water; for terrestrial feeding they can use (different from Testudo species) alternative to lingual food uptake a kind of inertial feeding mechanism; the tongue of these species is small enough to allow aquatic feeding by generating effective suction. Box turtles are supposed to be predecessors of recent terrestrial tortoises. It should be discussed if a semi-aquatic mechanism as seen in Cuora, could have evolved already at the very beginning of chelonian evolution, e.g., during the first transition from a terrestrial to an aquatic environment, or if it emerged much later in turtle history at the reconquering of the terrestrial habitat.

Beisser, CJ. & J. Weisgram (2001)
Dorsal tongue morphology and lingual glands in chelonians
Journal of Morphology 205: 3; p. 205 (Abstract).
(Poster at the 6. International Congress of Vertebrate Morphology; Jena, 21. 7. - 26. 7. 2001)

Within this study, several different turtle species were examined by means of light microscopy and scanning electron microscopy with respect to its dorsal tongue morphology. Results were set in relation with the species' life circumstances.
It could be shown that dorsal tongue morphology ranges from a very small, functional absent tongue in highly aquatic species (Chelus fimbriatus) via a very flat tongue topography without lingual glands (Acanthochelys pallidipectoris) to gradually higher and ridge-like papillae with beginning formation of glandular structures in semi-aquatic (Pelusios castaneus) and intermediate species (Trachemys scripta elegans). In semi-terrestrial species (Cuora amboinensis), already well-developed glandular regions can be found. The other endpoint of variety is resembled by very high and columnar papillae with distinct mucus glands in terrestrial (Rhinoclemmys pulcherrima) or highly terrestrial animals (Testudo hermanni).
Thus, tongue morphology correlates to a high degree with the species' life circumstances and with the feeding patterns primarily used by the animals: Highly aquatic species, using suction as the main mechanism for food uptake, try to reduce their tongue or at least keep it very small to prevent hindrance of the water flow during feeding process. The more a turtle species occupies terrestrial habitats, the more it uses terrestrial feeding patterns such as lingual feeding, where a well developed tongue morphology and lingual glands are necessary for food uptake and bolus formation.

see the whole poster as *.gif ! (980kb)

Beisser, CJ., Lemell, P. & J. Weisgram (2004)
The dorsal lingual epithelium of Rhinoclemmys pulcherrima incisia (Chelonia, Cryptodira).
The Anatomical Record Part A 277A: 227-235.

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.