Tongue Pad Research Articles

A tongue for all seasons: extreme phenotypic flexibility in salamandrid newts

Many organisms faced with seasonally fluctuating abiotic and biotic conditions respond by altering their phenotype to account for the demands of environmental changes. Here we discovered that newts, which switch seasonally between an aquatic and terrestrial lifestyle, grow a complex adhesive system on their tongue pad consisting of slender lingual papillae and mucus-producing cells to increase the efficiency of prey capture as they move from water onto land. The adhesive system is reduced again as newts switch back to their aquatic stage, where they use suction to capture prey. As suction performance is also enhanced seasonally by reshaping of the mouth due to the growth of labial lobes, our results show that newts are exceptional in exhibiting phenotypic flexibility in two alternating components (i.e. tongue pad and labial lobes) within a single functional system, and suggest that this form of phenotypic flexibility demands complex genetic regulation.

Lingual structural pattern of juvenile Chameleon, Chameleo chameleon

It is belong to the order Squamata, family, Chamaeleonidae. They have characteristic features of tongue protrusion during capturing prey attracts many research works and assay its velocity during protrusion. Yet little studies touched the anatomical and histological feature of the juvenile tongue and especially the middle tongue region involved in the tongue elongation, the present study aimed to focus on the histological structure of the mid-tongue and clarify its role in projection of the tongue as well as the glandular structure, keratinization of lingual epithelium and proliferation capacity of the fore-tongue region in relation with their feeding habits during the juvenile age. Juvenile Chameleo chameleon are collected from Abu Rawash, north of Giza Governorate, Egypt during summer 2015. Three juvenile developmental stages are used in the present study and categorized according to the gross morphological criteria of head, abdomen and limb lengths. The tongue and hyoid apparatus were removed and photographed. Histological, immunohistochemistry of cytokeratin and stem cell factor and scanning electronic microscopic investigations were carried out on the fore-tongue region, meanwhile only histological studies were done for the median tongue region. Morphometric assessments of number and length of lingual papillae and grades of cytokeratin and stem cell expression were done. Histologically, the dorsal lingual mucosa of the fore-tongue possessed different pattern of lingual papillae including finger-like, club, cubical, biforked and multi-branched papillae. The finger-like papillae are more abundant compared to the other types. The lamina propria of anterior median tongue pad are more glandular and exhibited abundant distribution of PAS-positive tubular glands and moderate alcian blue staining affinity of both alveolar and branched alveolar glands. There is no detected keratinization of the lingual epithelium. Stem cell factor appeared denser on the lingual mucosa and cell boundaries of glandular tissues. The mid-tongue region possessed a central cartilaginous core outlined by double layers of connective tissue coat and longitudinal and circular muscle fibers which give the power of protrusion of tongue. It is the first time to record the presence of cartilaginous elements in the mid-tongue region of chameleon. Finally the authors concluded that the juvenile stages of common chameleon exhibited striking cartilaginous inner compartment of the med-tongue and glandular fore-tongue adapted for capturing prey coincides with high proliferated activities and presence of different kinds of non-keratinized lingual papillae.

Selection of Biopsy Site for Patients with Systematic Amyloidosis.

Objective To evaluate the sensitivities of various biopsy methods for the diagnosis of systematic amyloidosis (SA). Methods The clinical data and biopsy results of 194 SA patients who were treated in Peking Union Medical College Hospital from January 2009 to June 2015 were retrospectively analyzed. Results The highest sensitivity was achieved by biopsy of affected organs,with renal biopsy 97.4%,heart biopsy 95.0% and liver biopsy 87.5%. Among non-invasive biopsy methods,tongue biopsy was found to be 75% sensitive,followed by gingiva biopsy at 57%,abdominal fat pad aspiration at 57%,rectum biopsy at 16%,and bone marrow examination at 8%. Combination of tongue and abdominal fat pad biopsy yielded a detection rate of 93.1%. Conclusions Biopsy of the involved organ has the highest sensitivity. However,combination of multiple non-invasive biopsy methods may has sensitivity comparable to organ biopsy and is safer and more convenient.

Tongue and taste organ development in the ontogeny of direct-developing salamander Plethodon cinereus (Lissamphibia: Plethodontidae).

The latest research on direct developing caecilian and anuran species indicate presence of only one generation of taste organs during their ontogeny. This is distinct from indirect developing batrachians studied thus far, which possess taste buds in larvae and anatomically distinct taste discs in metamorphs. This study is a description of the tongue and taste organ morphology and development in direct developing salamander Plethodon cinereus (Plethodontidae) using histology and electron microscopy techniques. The results reveal two distinct stages tongue morphology (primary and secondary), similar to metamorphic urodeles, although only one stage of taste organ morphology. Taste disc sensory zones emerge on the surface of the oropharyngeal epithelium by the end of embryonic development, which coincides with maturation of the soft tongue. Taste organs occur in the epithelium of the tongue pad (where they are situated on the dermal papillae), the palate and the inner surface of the mandible and the maxilla. Plethodon cinereus embryos only possess taste disc type taste organs. Similar to the direct developing anuran Eleutherodactylus coqui (Eleutherodactylidae), these salamanders do not recapitulate larval taste bud morphology as an embryo. The lack of taste bud formation is probably a broadly distributed feature characteristic to direct developing batrachians. J. Morphol. 277:906-915, 2016. © 2016 Wiley Periodicals, Inc.

The epithelia of the protrusible tongue of Eurycea longicauda guttolineata (Hoolbrook 1838) (Urodela: Plethodontidae).

In this study the lingual and sublingual glands, the lingual stem and the epithelial surface of the protrusible secondary tongue were investigated by light, scanning and transmission electron microscopy. The quality of the secretions of the epithelia was characterized histochemically. The lingual epithelium is formed by superficial (pavement) and goblet cells and at the margin of the tongue pad are also regions covered by ciliated cells. On the dorsal part of the tongue there are goblet cells of type A with mainly acidic secretions and of type B containing neutral secretions. Most of the goblet cells on the ventral side of the tongue (hypoglottis) show a strong alcian blue/PAS positive reaction (type I) and some produce neutral secretions (type II). The glandular cells of the lingual gland react positively to alcian blue and PAS in the apical region of the gland. In contrast there is only alcian blue-positive staining in the basal part of the gland. The size and complexity of the inclusion bodies of the secretory granules increase in a basal direction. In addition, there are ciliated cells in the glandular epithelium. Although the epithelium of the lingual stem is thin, it is double-layered. The cell types observed in this region are identical to those of the ventral part of the protrusible tongue. At the margin of the sublingual gland are trough-like structures. In the center, tubular parts are observed. The cells of this gland are stain strongly with alcian blue (pH 1.0) mainly in the basal part of the gland. The results of this are compared to the tongue pad and the lingual gland of Salamandra salamandra and Ambystoma mexicanum.

The mechanics of prey prehension in chameleons.

Iguanian lizards generally use their tongue to capture prey. Because lingual prehension is based on surface phenomena (wet adhesion, interlocking), the maximal prey size that can be captured is small. However, published records show that prey items eaten by chameleons include small vertebrates such as lizards and birds, indicating that these lizards are using a different prey prehension mechanism. Using high-speed video recordings, cineradiography, electromyography, nerve transection and stimulation experiments, we investigated the function of the tongue during prey capture. The results of these experiments indicate that chameleons have modified the primitive iguanian system by including a suction component in their prehension mechanism. Suction is generated by the activity of two modified intrinsic tongue muscles that pull the tongue pad inwards. Moreover, we demonstrate that the mechanism described here is a prerequisite for successful feeding.

Evolutionary Mechanics of Protrusible Tentacles and Tongues

This paper provides a comparison at multiple levels of structural organization of the biomechanics of protrusible muscular systems with different origins and phylogenetic history. The high-performance prey capture tentacles in squid, the tongues of frogs and salamanders, and the tongue of the chameleon are used as examples. The tentacles of squid are muscular organs that lack bony elements. They are rapidly elongated during prey capture(typical extension time 25 ms, peak acceleration of approximately 250 m.s › 2 ) by extensor muscles that have remarkably short sarcomeres (myosin e laments are only 0.5 to 1.0 mm, compared with 1.6 mm in vertebrates). Short sarcomeres generate only relatively small forces, but relatively high absolute strain rates for a given intere lamentary sliding velocity(at low external loads). A forward dynamics model (VAN LEEUWEN & KIER, 1997) predicts the movements of the tentacles with reasonable accuracy and predicts also that the short sarcomeres provide optimal extension velocity. Several frogs (Hemisotidae and Microhylidae) have a similar extension mechanism in their tongue (denoted as hydrostatic elongators by NISHIKAWA, 1999b) to that found in the tentacles of squid. The extension performance is, however, limited relative to that observed in squid. This can be explained by two factors. First, the extensor e bres run in one direction only, while in the squid the e bres are arranged in circumferential arcs as well as in two other e bre groups that run at right angles to each other. The unidirectional e bre orientation results in a smaller extension for a given shortening of the extensor e bres than observed in the tentacle. Second, the myosin e laments in the extensor muscle of the frog tongue are similar to those found in other vertebrate skeletal muscle. It is likely that the e lament lengths are not optimised for a high peak extension velocity although data are lacking thus far. These limitations have been circumvented by several groups of frog (Bufonidae, Ranidae and others) that ‘throw’ their tongue out of the mouth by a rapid jaw movement (inertial elongators). The ballistic tongues of many plethodontid salamanders extend in less than 10 ms. The most extreme performance is found in Hydromantes supramontis, which elongates the tongue up to 80% of body length. The paired cylindrical protractor muscles envelope two elongate epibranchials, the posterior ‘legs’ of the tongue skeleton. The complete tongue skeleton is projected with the tongue pad. The normal stress of the protractor muscle on

Modulation of prey-capture behavior in the plethodontid salamander Ensatina eschscholtzii

The hypothesis that salamander prey-capture behavior is highly stereotyped was tested in the plethodontid salamander Ensatina eschscholtzii using high-speed videography and kinematic analysis of feedings on two types of prey (waxworms and termites). The results show that E. eschscholtzii is capable of modulating the timing and magnitude of tongue and jaw movements in response to prey type. Feedings on waxworms, the larger prey, were characterized by shorter durations and higher velocities of tongue and jaw movements compared with feedings on termites, particularly in the latter portion of the feeding sequence (i.e. after prey contact). To test the hypothesis that sensory feedback through the tongue pad plays a role in modulating feeding movements in response to prey type, the ramus lingualis of the glossopharyngeal nerve (cranial nerve IX), which is known to carry sensory information from the tongue pad in salamanders, was transected bilaterally. This experimental deafferentation of the tongue pad had no effect on the degree or direction of differences in feeding kinematics across prey type. These results refute the glossopharyngeal feedback hypothesis, but are consistent with the hypothesis that E. eschscholtzii responds more vigorously to larger prey by assessing prey size visually.

Mechanisms of tongue protraction and narial closure in the marine toad Bufo marinus.

Electromyography, kinematic analysis, muscle stimulation and denervation techniques were used to investigate the muscular mechanisms of narial closure during breathing and of tongue protraction during prey capture in the marine toad Bufo marinus. Toads were video-taped during breathing and feeding under a variety of conditions: before surgery, after unilateral or bilateral denervation of the M. submentalis, and after unilateral or bilateral denervation of the Mm. genioglossus basalis and medialis. Deeply anesthetized toads were video-taped during stimulation of several cranial muscles, and electromyograms were recorded from the M. submentalis during feeding before and after its denervation. Bufo marinus differs from many other anurans in having a relatively long tongue that experiences large accelerations (> 31 g) during protraction. Tongue protraction occurs in two phases: an early phase during which the lingual tip moves upward and forward relative to the mandibular tip as the tongue shortens, and a later phase during which the lingual tip moves downward and forward relative to the mandibular tip as the tongue elongates under its own momentum. Relative to an external reference, the lingual tip follows a straight trajectory from mouth to prey, which depends critically upon precise coordination of tongue and jaw movements. The M. submentalis is necessary for normal tongue protraction during feeding. In contrast, the Mm. genioglossus basalis and medialis are necessary for forward movement of the tongue pad over the symphysis. In B. marinus, a simple anatomical change (elongation of the tongue) has functional consequences (inertial elongation) that profoundly affect the mechanisms of neuromuscular control. Though seldom studied, it seems likely that morphological evolution has had a profound influence on mechanisms of motor control in animals generally.

Structure and function of the hyolingual system in Hynobius and its bearing on the evolution of prey capture in terrestrial salamanders.

The Hynobiidae is generally regarded as the most phylogenetically basal and least derived extant family of terrestrial salamanders. As in the other families of terrestrial salamanders, prey capture in the Hynobiidae is accomplished by lingual prehension. In Hynobius, the prey capture system appears to be a mosaic of derived and primitive features. This, in conjunction with previous studies, suggests that the hyolingual systems of all families of terrestrial salamanders have evolved various degrees of specialization since the appearance of the common ancestral condition. We propose that the generalized feeding system for the extant terrestrial salamanders includes a hyolingual skeleton comprised of one basibranchial, one pair of radial or radial-like structures, two pairs of ceratobranchials, two pairs of epibranchials, one pair of ceratohyals, and one urohyal arranged in a configuration similar to that of Hynobius; a simple, sac-like secondary tongue pad; a lift and thrust system of tongue projection; a four-part gape cycle; and a forward head and body surge. Modifications to this general plan, previously described for the disparate families, include various changes in the size, shape, and definition of the tongue pad, changes in the specific types of structures and configurations in the anterior hyolingual skeleton, secondary ossification in the posterior hyolingual skeleton, the appearance of various protrusion, projection, and flipping systems for tongue protraction, simplification of the kinematic gape profile, and loss of the forward head and body surge. The evolutionary trends in these modifications have provided a rich data set from which much phylogenetic information has been inferred. © 1996 Wiley-Liss, Inc.

Mechanism of tongue protraction during prey capture in the spadefoot toad Spea multiplicata (Anura: Pelobatidae)

Recent studies have used muscle denervation experiments to examine the function of muscles during feeding in frogs. By comparing the results of denervation experiments among taxa, it is possible to identify evolutionary changes in muscle function. The purpose of this study was to examine the function of jaw and tongue muscles during prey capture in Spea multiplicata, a representative of the superorder Mesobatrachia. All members of this group possess a disjunct hyoid apparatus. We predicted that Spea would possess a novel mechanism of tongue protraction on the basis of its hyoid morphology. High-speed video motion analysis and muscle denervation were used to study the feeding behavior and mechanism of tongue protraction in Spea. Although Spea possesses a relatively long tongue, its feeding behavior is similar to that of short-tongued frogs of similar body size. Denervation of the m. submentalis had no effect on feeding behavior. When the m. geniohyoideus was denervated, the tongue pad was raised and moved forward slightly, but did not leave the mouth. When the m. genioglossus was denervated, the tongue pad was raised slightly, but no forward movement of the tongue occurred. A similar result was obtained after the mm. genioglossus and geniohyoideus were denervated simultaneously. Thus, both the mm. genioglossus and geniohyoideus are necessary for normal tongue protraction in Spea. In contrast, only the m. genioglossus is necessary for normal tongue protraction in archaeobatrachians and neobatrachians. We hypothesize that the disjunct hyoid is responsible for the greater role of hyoid movement during feeding in mesobatrachians.

Variation in the feeding kinematics of mole salamanders (Ambystomatidae:Ambystoma)

High-speed cinematography was used to investigate the prey-capture kinematics of six species of mole salamanders (Ambystomatidae). We compared the feeding behavior of the subgenus Ambystoma (A. californiense and A. macrodactylum) with that of the subgenus Linguaelapsus (A. mabeei, A. texanum, A. annulatum, and A. cingulatum). Prey capture by all six species is characterized by a 3-part gape cycle (a period of rapid mouth opening prior to extraoral tongue protraction, followed by a period of relatively stable gape angle during extraoral tongue protraction and retraction, followed by a period of rapid mouth closure), a tongue-extension cycle (protraction and retraction), and anterior head–body displacement. Among the six species, two distinct modes of prey capture are evident: (1) the Ambystoma mode (A. californiense, A. macrodactylum, A. mabeei, and A. texanum), and (2) the Linguaelapsus mode (A. annulatum and A. cingulatum). Most differences in prey-capture kinematics between the two modes are primarily differences of degree rather than the addition or loss of unique behaviors, and include a general reduction in the gape angles and a general increase in the elapsed times associated with specific events in the Linguaelapsus mode. We hypothesize that these differences are primarily the result of a prolonged period of tongue protraction in the Linguaelapsus mode during which the glandular tongue pad is fitted to the prey. In addition to differing from each other, the gape profiles of the ambystomatid subgenera differ markedly from the 4-part gape profiles of plethodontids and salamandrids.

Kinematics of prey capture in the tailed frog Ascaphus truei (Anura: Ascaphidae)

The kinematics of prey capture by Ascaphus truei was investigated. High-speed films (100 fps) of 13 successful and one unsuccessful prey capture sequences from six adult frogs were analysed. Ascaphus, the sister group of all living frogs, shares several aspects of feeding kinematics, including rotation of the tongue pad about the mandibular symphysis and mandibular bending during mouth opening and closing, with more derived frogs such as Bufo marinus. The times required for tongue retraction, mouth opening and closing are similar in Ascaphus and Bufo. However, because Bufo is much larger and protracts its tongue much farther than Ascaphus, the velocities of tongue retraction, mouth opening and mouth closing are relatively lower in Ascaphus than in Bufo. Differences in prey capture between Ascaphus and Bufo marinus are (1) the distance of tongue protraction is less in Ascaphus (±0.5 cm) than in Bufo (c. 2 cm); and (2) lunging of the whole body is more pronounced in Ascaphus. Prey capture is highly variable in Ascaphus. An intraoral transport sequence is sometimes (7 of 14 observations) inserted into the prey capture cycle before the completion of mouth closing. The gape cycles range from 80–150 ms for sequences with no oral transport and from 130–280 ms for sequences with oral transport. Also, the time required for tongue retraction is significantly longer in the unsuccessful capture attempt. This variability is generally greater than that observed during prey capture in salamanders, and suggests that frogs and salamanders may differ in the importance of sensory feedback in coordinating prey capture.

Hyolingual feeding systems of the Plethodontidae: Comparative kinematics of prey capture by salamanders with free and attached tongues

AbstractHigh‐speed cinematography (500 fps) was used to analyze quantitatively the kinematics of terrestrial prey capture in Bolitoglossa occidentalis, B. mexicana, Ensatina esch‐scholtzii, Plethodon glutinosus, Desmognathus quadramaculatus, Hynobius kimurae, and H. nebulosus. The gape cycle of these salamanders is highly stereotyped. In B. occidentalis the mouth is opened by a combination of cranial elevation and mandibular depression. The gape increases dramatically during tongue retraction, thus allowing the prey to be delivered to the rear of the oral cavity without being impeded by the marginal teeth. The absence of a feeding function for these teeth apparently has resulted in their reduction and/or morphological alteration in some bolitoglos‐sines. Observed differences in jaw rotation between successful and unsuccessful prey capture attempts appear to be biomechanical phenomena and not adjustments by the salamander in response to neural feedback.Tongue projection is most rapid and highly accurate in the two bolitoglossines and Ensatina. The distance to which the tongue can be protracted from the mouth is 7% snout‐vent length in D. quadramaculatus, P. glutinosus, H. kimurae, and H. nebulosus (attached protrusible tongue); 15% in E. eschscholtzii (attached projectile tongue); and 30% in B. occidentalis (free projectile tongue). Even though tongue protraction is significantly faster in salamanders with projectile tongues than those with protrusible tongues, the range of times for the entire gape cycle is generally similar for all salamanders (ca. 100 ms). However, less derived salamanders spend a shorter period preparing the tongue for firing and more time in its projection than E. eschscholtzii and B. occidentalis. One obvious advantage for increasing the speed of tongue protraction is that it decreases the prey's available escape time. In the supergenus Bolitoglossa prey are limited to small, active invertebrates by a combination of stereotyped feeding behavior, a small tongue pad, and a lightweight hyolingual apparatus that is projected extremely fast.While all terrestrial salamanders possess the same basic feeding system, the bolitoglossines have evolved an impressive array of unique specializations for capturing small, rapidly moving prey. This suite of characters has enabled the tribe to radiate rapidly into a vast variety of microhabitats.

Quantitative analysis of feeding kinematics in dusky salamanders (Desmognathus)

Gape formation by the dusky salamander (Desmognathus) involves both upper and lower jaws and occurs in a manner similar to that of other terrestrial salamanders. As Desmognathus opens its mouth, ventral rotation of the mandibles is restricted but not stopped by the atlas–mandibular ligaments; the lower jaw is not propelled anteriorly. Tongue protraction, well beyond the mandibular symphysis, is always a major component of prey capture by this genus. After the sticky tongue pad has made contact with the prey, the salamander's head surges forward and the pad is rapidly retracted with the prey item attached. Aided by a unique suite of characters the mouth then snaps shut with considerable force. Our study supports the premise that Desmognathus is no different from most, if not all, terrestrial salamanders in its employment of tongue projection as a major feature in prey capture. We argue that the primary selective force for the unique configuration of desmognathine cephalic structures was enhancement of the ability of these small salamanders to capture relatively large prey without an increase in the size of the head and body.

Tongue function in the salamander Bolitoglossa occidentalis

Many plethodontid salamanders feed by means of tongue projection. Aspects of this mechanism were studied in the species Bolitoglossa occidentalis under laboratory conditions. Drosophila were presented at varying controlled distances from the animal. The force and duration of tongue contact with the prey, plus the EMG activity in the tongue protractor and tongue retractor muscles, were recorded. Both force and duration of contact decreased with increasing distance of tongue projection. Various measures of protractor muscle EMG activity were independent of projection distance. Protractor and retractor muscle activities were synchronous and continued throughout the projection-retraction cycle. The latency of a ‘tongue pad to retractor muscle’ reflex was greater than the shortest durations of tongue contact. Furthermore, the longest durations of contact were always associated with the greatest forces exerted by the tongue. In the light of these findings, a model is proposed in which projection-retraction is co-ordinated by properties of the peripheral structures rather than by those of the central nervous system.

The Morphology and Evolution of the Tongue and Associated Structures in Salamanders and Newts (Family Salamandridae)

Within the family Salamandridae, a relatively great diversity of feeding mechanisms is found. Dissections of the jaw, tongue, and throat musculature combined with serial section analysis, studies of osteology, and behavioral observations provide data which are used to analyze functional morphology of feeding mechanisms among the 14 genera. There are two distinct classes of feeding mechanisms in the family. One class, characterized by those species with tongues, involves specializations associated primarily with feeding in aquatic habitats. Included are those salamandrids which are aquatic at least during the breeding season, Tylototriton, Pleurodeles, Triturus, Neurergus, Euproctus, Paramesotriton, Cynops, Hypselotriton, Pachytriton, Taricha, and Notophthalmus. These genera utilize the gape and suck method of feeding in aquatic situations, but most utilize a modified jaw-feeding mechanism on land. Some of the genera (e. g., Pachytriton) are exclusively aquatic, and in these specializations for aquatic feeding are extreme. Tylototriton and Pleurodeles are much more generalized than the other genera. A general trend in genera with water tongues is for an elaboration of the posterior parts of the hyobranchial apparatus and associated musculature together with a reduction in structure and function of the anterior parts of the functional unit. In addition, the hyobranchial apparatus becomes increasingly ossified and rigid as specializations for gape and suck feeding, such as throat expansion, increase. Land tongues are found in Salamandra, Chioglossa, and Salamandrina, and are especially highly developed in the last two. These genera are specialized for feeding in terrestrial situations. Here the general trend is for an elaboration of the anterior parts of the functional unit, especially the tongue pad, and a reduction in the posterior parts. The hyobranchial apparatus is quite flexible and permits extensive flipping of the tongue pad from the mouth. Prey is captured through tongue pad flipping, but in quite a different manner than in tongue feeders in other families.