Comparative observations on lingual papillae and their connective tissue cores in three primates. A scanning electron microscopic study

The 3-D structure of the connective tissue cores (CTCs) of the lingual papillae in three primates (treeshrew, crab-eating monkey and man) was observed by scanning electron microscopy. Each filiform papilla has some slender protrusions on the top in the three kinds of primates. After removal of the epithelium, the CTC of the filiform papillae has a columnar primary core with some rod shaped secondary protrusions whose number and size vary among the three species. The number of secondary protrusions on the filiform CTC is generally small in the treeshrew and is the greatest in man. The stereo structure of the filiform CTC is fundamentally similar in all these three species and is different from those of other animal orders (i.e. Insectivora, Rodentia etc.). The fungiform CTC in man as well as in the crab-eating monkey is coralliform in shape and branched several times with small depressions for taste buds on the top of each one, though there were some differences between the two species in stereo structure. On the other hand, the fungiform CTC in the treeshrew was columnar in shape and was rather similar to that of Insectivora and Rodentia. In the treeshrew there are several finger-like processes in the region where foliate papillae are located in man as well as in the crab-eating monkey.     

Morphology of the lingual papillae in the sitatunga

We examined the dorsal lingual surfaces of an adult sitatunga (Tragelaphus spekei) by scanning electron microscopy. Filiform, fungiform and vallate papillae were observed. The filiform papillae consisted of a larger main papilla and smaller secondary papillae. The filiform papilla contained connective tissue core consisting of several processes. The fungiform papillae were round in shape. The connective tissue core of the fungiform papilla was flower-bud shaped. Lenticular papillae were limited on the torus lingua. The connective tissue core of the lenticular papilla consisted of numerous small spines, or these spines and rod-shaped processes. The vallate papillae were flattened-oval shaped and the papillae were surrounded by a circular trench. The connective tissue core of the vallate papilla was covered with numerous small spines. These findings indicate that the tongue of the sitatunga is similar to that of the blackbuck and Barbary sheep.     

Morphology of the lingual papillae in the Japanese marten

The dorsal lingual surfaces of two adult Japanese marten (Martes melampus) were examined by scanning electron microscopy (SEM). Filiform, fungiform, vallate and foliate papillae were observed. A small filiform papilla on the apical surface of the tongue had several pointed processes. A small filiform papilla contained the connective tissue core consisting of several small processes. A large filiform papilla of the lingual body consisted of a main papilla and some secondary papillae. A large filiform papilla contained the connective tissue core consisting of processes of various size. The fungiform papillae are round in shape. The connective tissue core of the fungiform papilla had a top with several round depressions. The four vallate papillae were located on both sides of the posterior end of the lingual body and each papilla was surrounded by groove and crescent pad. A zigzag surface structure appeared on the connective tissue core of the vallate papilla. The foliate papillae were seen on the dorsolateral aspect of the tongue and some ridges and grooves were exposed reciprocally. A zigzag surface structures appeared on the connective tissue cores of the ridges of the foliate papillae.     

Morphology of the lingual papillae and their connective tissue cores in the cape hyrax

The dorsal lingual surfaces of four adult cape hyraxes (Procavia capensis) were examined by scanning electron microscopy (SEM). Filiform, fungiform and foliate papillae were observed. The lingual body had lingual torus on the posterior third. In the lateral sides of the tongue large fungiform papillae were observed and in the lateral sides of the torus very developmental foliate papillae were observed. Many fungiform papillae were observed in the ventral surface of the lingual apex. No vallate papillae were seen on the dorsal surface. The filiform papilla on the apical surface of the tongue had shovel-shaped papilla. The filiform papilla contained the connective tissue core consisting of some processes. The connective tissue core of the fungiform papillae was floral bud in shape. In the surface of the lingual torus numerous dome-shaped papillae are found. The dome-shaped papilla contained the connective tissue core consisting of a zigzag surface structure and the connective tissue core is surrounded by the processes of various sizes. In the surface of the lingual root numerous openings of the lingual glands were found. Around the glandular openings connective tissue ridges formed circular sheaths. In the lateral sides of the tongue large fungiform papillae were round in shape. The connective tissue core of the fungiform papilla was floral bud in shape. The foliate papillae were seen on the dorsolateral aspect of the tongue and some ridges and grooves were exposed reciprocally. Many small protrusions appeared on the connective tissue core of the ridge of the foliate papilla. These findings suggested that in the structure of the lingual papillae of the cape hyrax there was intermediate type between Rodentia and Artiodactyla.     

Comparative morphological study of the lingual papillae and their connective tissue cores of the koala

The stereo structure of each lingual papilla of the koala has a similar structure to that of various other animal species: the koala has a lingual prominence (intermolar prominence) with larger filiform papillae. (A lingual prominence is a characteristic in herbivorous animals.) The external form and connective tissue core (CTC) of the filiform papillae of koalas consist of one large main process and several smaller accessory processes. (These are similar to carnivorous animals.) Fungiform CTC have a thick dome-like structure, with several taste buds on the top. There are three vallate papillae: one central midline and two laterally located vallate papillae. The central vallate papilla has a posterior pouch lined with ciliated and non-ciliated epithelial cells. Long conical papillae are distributed in the posterior lateral area where foliate papillae are distributed in many other animal species. (Finger-like papillae are seen in dog and cat instead of foliate papillae.) It may be suggested that the tongue of the koala evolved in a special environment in Australia. Even though it has still retained special features similar to those of carnivorous cats and dogs it has evolved to resemble the tongues of herbivorous animals.     

Morphology of the lingual papillae in the roan antelope

We examined the dorsal lingual surfaces of an adult roan antelope (Hippotragus equinus) by scanning electron microscopy. Filiform, fungiform and vallate papillae were observed. The filiform papillae consisted of a larger main papilla and smaller secondary papillae. A top of the connective tissue core of the filiform papilla showed several depressions. The connective tissue core of the papilla with a long process was rarely observed. The fungiform papillae were round in shape. The connective tissue core of the fungiform papilla was flower-bud shaped. The lenticular papillae of large size were limited on the torus lingua. The connective tissue core of the lenticular papilla consisted of numerous small spines. The vallate papillae were located on both sides of the posterolateral aspects. The vallate papillae were flattened oval shaped and the papillae are surrounded by circular trench. The connective tissue core of the vallate papilla was covered with numerous small spines.     

Morphology of the lingual papillae in the raccoon dog and fox

The dorsal lingual surfaces of the raccoon dogs (Nyctereutes procyonoides) and fox (Vulpes vulpes japonica) were examined by scanning electron microscopical (SEM) observations. The distribution and type of the lingual papillae found in the raccoon dog were similar to those in the fox. Filiform, fungiform, foliate and vallate papillae were observed. The filiform papillae were distributed over the entire dosal surface of the tongue. Each filiform papilla on the apical surface of the tongue had several pointed processes. The filiform papillae of the lingual body consisted of a main papilla and some secondary papillae. The fungiform papillae were present rounded bodies, and more densely distributed on the lingual apex. The foliate papillae were seen on the dorsolateral aspect of the tongue. The vallate papillae were located on both sides of the posterior end of the lingual body. Each papilla was surrounded by groove and crescent pad. On the periphery of the papillae, large conical papillae were observed.     

Light and scanning electron microscopic study on the lingual papillae and their connective tissue cores of the Cape hyrax Procavia capensis

We examined the epithelial surface and connective tissue cores (CTCs) of each lingual papilla on the Paenungulata, Cape hyrax (Procavia capensis), by scanning electron microscopy and light microscopy. The tongue consisted of a lingual apex, lingual body and lingual root. Filiform, fungiform and foliate papillae were observed on the dorsal surface of the tongue; however, fungiform papillae were quite diminished on the lingual prominence. Moreover, no clearly distinguishable vallate papillae were found on the tongue. Instead of vallate papillae, numerous dome-like large fungiform papillae were arranged in a row just in front of the rather large foliate papillae. Foliate papillae were situated in the one-third postero-lateral margin of the lingual body. The epithelium of filiform papillae was covered by a keratinized layer with kerato-hyaline granules, whereas weak keratinization was observed on the interpapillary epithelium. The external surface of the filiform papillae was conical in shape. CTCs of the filiform papillae were seen as a hood-like core with a semicircular concavity in the anterior portion of each core. Large filiform papillae were distributed on the lingual prominence. The CTCs of large filiform papillae after exfoliation of their epithelium consisted of a concave primary core and were associated with several small protrusions. The surface of fungiform papillae was smooth and dome-like. After removal of the epithelium, CTCs appeared as a flower bud-like primary core and were associated with several protrusions that were arranged on the rim of the primary core. Several taste buds were found on the top of the dorsal part of the epithelium of both fungiform and large fungiform papillae. Well-developed foliate papillae were seen and numerous taste buds could be observed in the lateral wall of the epithelium in a slit-like groove. The morphological characteristics of the tongue of the Cape hyrax had similarities with other Paenungulata such as Sirenia. However, three-dimensional characteristics, especially CTCs of lingual papillae, exhibited multiple similarities with rodents, insectivores and artiodactyls.     

Morphology of the lingual papillae in the Patagonian cavy

We examined the dorsal lingual surfaces of an adult Patagonian cavy (Dolichotis patagonum) by scanning electron microscopy. The tongue of the Patagonian cavy is about 8 cm long and the lingual body had lingual prominence on the posterior third. There were no fungiform papillae in the lingual dorsal surface. The fungiform papillae were observed in both lateral sides of the lingual apex. The filiform papilla of the lingual body consisted of a large conical papilla. The connective tissue core of the filiform papilla showed many slender processes. The fungiform papillae were round in shape. The connective tissue core of the fungiform papilla was flower-bud shaped. Two vallate papillae were located on between lingual body and root, and insert in two grooves. The connective tissue core of the vallate papilla was covered with numerous small spines. Many foliate papillae were observed on the posterolateral regions of the tongue. After removing epithelium from the foliate papillae many vertical depressions became apparent. These findings suggest that in the structure of the lingual papillae of the Patagonian cavy there is similar to that of the capybara.     

Scanning electron microscopic study on the lingual papillae of the Japanese insectivora

The tongue and lingual papillae of the Japanese Insectivora, the Shinto shrew (Sorex caecuiens saevus), the long-clawed shrew (S. unguiculatus), the dsinezumi shrew (Crocidura dsinezumi dsinezumi) and the Japanese water shrew (Chimarrogale himalyica platycephala), were observed by scanning electron microscope. The tongue of these animals had two vallate papillae. In two species of the Sorex a papilla in the vallate papilla was surrounded by two separated trenches, but in the other species it was surrounded by only a continuous trench and a clear vallum. The fungiform papillae in the Sorex were less developed than those of the other species. In the Sorex and Crocidura, there was no filiform papilla on the lingual apex. These genera, however, have papillary projections in the margin of the lingual apex. The results of this investigation suggest that the Sorex and Crocidura indicate an ancient form of the mammalian tongue. These characters, furthermore, were compared among seven species in six genera added three species observed by Kobayashi et al. (1983) to this study.     

Comparative morphological study on the lingual papillae and their connective tissue cores in rabbits

The morphological structure of the lingual papillae and their connective tissue cores (CTC) in a rabbit were studied using LM and SEM and were compared to that of other animal species. Externally, the filiform papillae distributed on the anterior surface of the dorsal tongue were short and conical with a round base and had a flat area on their anterior upper half. The CTC of the conical filiform papillae had a roughly triangular plate-like structure with a round top. Several small round protrusions were found on both inclined planes of the triangle. Spearhead-like filiform papillae were distributed on the anterior edge of the lingual prominence and branched filiform papillae were on the posteriorly wide area of the prominence. These papillae on the prominence had a slightly ramified CTC that differed from that of the CTC of the conical filiform papillae distributed on the anterior tongue. Dome-like fungiform papillae were distributed among the conical filiform papillae of the anterior tongue and had a CTC with a roundish structure that was almost but, not quite spherical in appearance with 1 to 10 small round concave indentations for taste buds on their upper surface. The foliate papillae had approximately 15 parallel ridges separated by grooves. These ridges contained a parallel thin plate-like CTC exhibited after removal of the epithelium. The vallate papilla was comprised of a spherical central papilla and had a circular wall with a flower-like CTC almost resembling a carnation. The stereostructure of the rabbit's filiform CTC are comparatively described as being morphologically in between those of rodents and those of the guinea pig and Japanese serow. Such evolution has probably occurred due to the species unique masticatory and gustatory needs and functions.     

Comparative morphological study on the lingual papillae and their connective tissue cores (CTC) in reeves’ muntjac deer (Muntiacus reevesi)

The lingual papillae and their connective tissue cores (CTC) from Reeves’ muntjac deers (herbivorous artiodactyla) were studied using light and scanning electron microscopy and then compared to those of other mammalian species. At the posterior portion of the tongue, the Reeves’ muntjac has a lingual prominence on which large conical papillae are distributed. On the dorsal surface of the anterior tongue, numerous filiform papillae were found. Externally, each filiform papilla consists of a rod-shaped main process and several small accessory processes. Their CTCs consist of 10 or more rod-shaped processes arranged in a horseshoe pattern and several posterior processes forming a small circular pattern. This structure is a common characteristic of artiodactyla, through which Reeves’ muntjac deer can be categorized in a position in the artiodactyla class lying between the bighorn sheep and the East African bongo. Fungiform papillae are distributed among the filiform papillae on the anterior portion of the tongue. Large fungiform papillae are also sparsely distributed on the lingual prominence and have several taste buds in the epithelium on the surface. Ten or more vallate papillae are distributed at the postero-lateral area of the lingual prominence and numerous taste buds are distributed in the epithelium of their side.     

Morphology of the dorsal lingual papillae in the bush dog (Speothos venaticus)

The dorsal lingual surface of a bush dog (Speothos venaticus) was examined by scanning electron microscopy (SEM). The tongue was about 7 cm in length. Filiform, fungiform and vallate papillae were found. The filiform papillae were distributed over the entire dorsal surface of the tongue. Each filiform papillae on the apical surface of the tongue had several conical processes, in the midportion were larger than those on the apex in size. In the region of the vallate papillae, the filiform papillae had not the conical processes and more larger than those on the midportion of the tongue. The fungiform papillae were present rounded bodies and more densely distributed on the tip of the lingual apex. There were 5 vallate papillae on both sides. The vallate papillae were located on both sides of the posterior end of the lingual body. Each papilla was surrounded by a groove and a crescent pad. In the dorsal surfaces of the papillae, small conical papillae were observed.     

Comparative morphological study on the stereo-structure of the lingual papillae and their connective tissue cores of the American beaver (Castor canadensis)

The lingual papillae and the connective tissue cores (CTC) of the American beaver were examined by light and scanning electron microscopy. The tongue of American beaver was about 9 cm in length, 3.5 cm in width, and has a lingual prominence. Four types of papillae (filiform, fungiform, vallate and foliate papillae) were observed. The filiform papillae can be classified into three types (filiform, large filiform and dorm-like papillae). Filiform papillae distributed on the anterior tongue and posterior of the lingual prominence consisted of a posterior thick main process and several small accessory processes. After removal of the epithelium, the CTCs of the filiform papillae had U-shaped, horseshoe-like primary cores with 10-15 rod-shaped small accessory cores. Large filiform papillae were distributed at the anterior margin of the lingual prominence. Dome-like papillae were distributed at the top of lingual prominence. Fungiform papillae were observed two types. Fungiform papillae, which were distributed at the anterior tongue, were round shaped. Fungiform papillae of the posterior of the lingual prominence were large and surrounded with a papillary groove. At the posterior of the tongue, three vallate papillae were arranged in a triangular pattern. Foliate papillae were on 22 to 25 parallel ridges and grooves.     

Scanning electron microscopy study of the tongue and lingual papillae of the California sea lion (Zalophus californianus californianus)

We observed the three-dimensional structures on the external surface and the connective tissue cores (CTCs) of the California sea lion (Zalophus californianus californianus), after exfoliation of the epithelium of the lingual papillae (filiform, fungiform, and vallate papillae), using scanning electron microscopy (SEM) and conventional light microscopy. Macroscopically, the tongue was V-shaped and its apex was rounded. At the posterior area of the tongue, five vallate papillae were arranged in a V shape. In the epithelium, numerous taste buds were distributed on the top of the vallate papillae. On the dorsal surface from the apex to the boundary between the anterior and posterior tongue, filiform papillae were densely distributed. The CTCs of the filiform papillae consisted of a main protrusion (primary core) and many small cores (secondary cores). From the apex to the anterior one-third of the tongue, dome-like fungiform papillae were densely distributed, whereas fewer were located at the posterior two-thirds of the tongue. Several taste buds were found in the epithelium on the fungiform papillae. The size of the filiform papillae gradually increased from the apex to the boundary between the anterior and posterior tongue. At the lingual radix, the conical papillae, which were bigger than any filiform papillae, were densely distributed. The morphological characteristics of the tongue of the California sea lion appear to have been transformed to adapt to an aquatic environment; however, they possess some structures similar to those of land mammals.     

Light and scanning electron microscopic study on the tongue and lingual papillae of the common raccoon, Procyon lotor

We observed the external surface and connective tissue cores (CTCs), after exfoliation of the epithelium of the lingual papillae (filiform, fungiform, foliate and vallate papillae) of the common raccoon (Procyon lotor) using scanning electron microscopy and light microscopy. The tongue was elongated and their two-third width was almost fixed. Numerous filiform papillae were distributed along the anterior two-thirds of the tongue and fungiform papillae were distributed between the filiform papillae. Eight vallate papillae that had a weak circumferential ridge were distributed in a V-shape in the posterior part of the tongue and numerous taste buds were observable in the circumferential furrows of vallate papillae. Weak fold-like foliate papillae were observable at the lateral edge in the posterior part of the tongue and a few salivary duct orifices were observable beneath the foliate papillae. An islet-like structure with numerous taste buds, was observable on the deep part of the salivary duct of foliate papillae. Large conical papillae were distributed at the posterior part and root of the tongue. After removal of epithelium, filiform papillae of CTCs were appeared to be a thumb or cone-like main core and associating several finger-like short accessory cores. These cores were surrounded an oval concavity. The main core was situated behind the concavity and associated with accessory cores. CTCs of fungiform papillae were cylinder-like with numerous vertically running ridges and with a few concavities seen at the top of the cores. CTCs of vallate papillae and their surrounded circumferential ridge were covered with numerous pimple-like protrusions. The lingual papillae of Common raccoon's tongue had morphological feature of carnivore species.     

The scanning electron microscopic study of lingual papillae in the silver fox (Vulpes vulpes fulva, Desmarest, 1820)

The tongues of adult silver foxes were studied using scanning electron microscopy. Five types of lingual papillae were found on the dorsal surface of the tongue. The most numerous papillae were filiform papillae covering the apex and body of the tongue. The filiform papillae on the anterior part of the tongue are divided into 1 main and 10-12 accessory processes. In the posterior part of the body of the tongue the number of accessory processes is reduced. Fungiform papillae are located between the filiform papillae. A cluster of 12 large fungiform papillae was found on the apex of the tongue. Conical papillae are located in the area of the vallate papillae and cover the posterior part of the root of the tongue. Their size increases towards the pharynx, where they are distributed more sparsely. In the silver foxes there were two pairs of vallate papillae. The wall surrounding each papilla and its gustatory trench forms partly connected 6-8 conical papillae. The foliate papillae on both margins of the tongue body are small and consist of 4-5 laminae. The distribution and type of lingual papillae found in the silver fox are similar to those in the other species belonging to the family Canidae.     

Three-dimensional architecture of the connective tissue papillae of the mouse tongue as viewed by scanning electron microscopy

The morphological relationship between lingual papillae and underlying connective tissue papillae of mouse was studied because it is conceivable that the differentiation of epithelium may be affected by its connective tissue. Tongues of adult male mice were fixed in formol or Karnovsky's fixative. After removal of the epithelium by long-term hydrochloric acid treatment at room temperature, the surface of the connective tissue papillae was observed by scanning electron microscopy. Connective tissue papillae that were fungiform in shape and which were distributed at the anterior part of the tongue showed barnacle-like protrusion after removal of the epithelium. Their surface was covered by numerous long filaments running vertically and there was a round depression on the top of each fungiform papilla that may be found to correspond to a taste bud when the results of light and electron microscopy are compared. Filiform papillae in a narrow sense were closely distributed in the anterior part of the tongue. They had a tapered tip declining posteriorly. Each filiform connective tissue papilla was conical in shape and had a round depression that slightly declined antero-downward, and a long narrow depression ran along the anterior edge of each connective tissue papilla. Large conical papillae which distributed at the anterior margin of the intermolar prominence had shovel-like connective tissue papillae which had a depression at the posterior surface unlike that of the filiform papillae. Branched papillae distributed in the posterior part of the prominence had a depression at the anterior surface. Under the light microscope, numerous keratohyaline granules were seen to be contained only in the posterior epithelial cell line of the large conical papillae distributed in the anterior margin of the prominence, while these granules were found only in the anterior epithelial cell line of both filiform and branched papillae. It became clear that the axes of each connective tissue papilla of large conical papillae distributed radically around a single midpoint. Connective tissue papillae of vallate papillae had a beehive-like shape and in follicate papillae there were several vertical elliptical gaps, seen when the epithelium was peeled from the connective tissue.     

Morphology of the dorsal lingual papillae in the barbary sheep, Ammotragus lervia

The dorsal lingual surface of a barbary sheep (Ammotragus lervia) was examined by scanning electron microscopy (SEM). The tongue was about 20 cm in length. There were about 30 vallate papillae on both sides. Filiform, conical, fungiform and vallate papillae were found. The filiform papillae were distributed over the entire dorsal surface of the tongue, excepted for the lingual torus where conical papillae were present. The fungiform papillae were present rounded bodies, and more densely distributed as compared to that of the lingual body on the tip and ventral surface of lingual apex. No foliate papillae were seen on the dorsal surface. The vallate papillae were located on both sides of the midline in the caudal part. Each papilla was surrounded by a groove. These findings indicate that the tongue of the barbary sheep is similar to that of the formosan serow, japanese serow and blackbuck.     

Light and Scanning Electron Microscopic Study on the Structure of the Lingual Papillae of the Feathertail Glider (Acrobates pygmeus,Burramyidae, Marsupialia)

The structure of the tongue of the marsupial feathertail glider (Acrobates pygmeus) was observed under a light and scanning electron microscope. The elongated tongue with a sharpened apex is ca. 10 mm in length. Only the posterior half of the tongue is attached to the bottom of the oral cavity by the frenulum, which facilitates considerable mobility of the anterior free part of the tongue. On the dorsal surface of the tongue, three types of lingual papillae were distinguished, that is, mechanical filiform papillae and gustatory fungiform and vallate papillae. The arrangement, shape, and size of filiform papillae and the direction of their keratinized processes change depending on the part of the tongue, so that the surface of the apex and the body of the tongue resembles a brush adapted to effective holding of semiliquid food and collection of pollen. The fungiform papillae have a single taste bud and are uniformly scattered between filiform papillae only on the anterior half of the tongue. On the smooth root of the tongue, three oval vallate papillae are arranged in the form of a triangle, similarly as it is the case in other marsupials. The posterior biggest vallate papilla is oriented perpendicularly to the smaller anterior papillae. The results of the study on the feathertail glider show that the special arrangement of lingual papillae is strongly adapted to feeding behavior of this nectar‐eating and frugivorous animal. Anat Rec, 290:1355–1365, 2007. © 2007 Wiley‐Liss, Inc.