Convergent evolution in feeding types: salivary gland mass differences in wild ruminant species

In the ongoing debate about divergent evolutionary morphophysiological adaptations of grazing and browsing ruminants, the size of the salivary glands has received special attention. Here, we report the most comprehensive dataset on ruminant salivary glands so far, with data on the Glandula parotis (n=62 species), Gl. mandibularis (n=61), Gl. buccalis ventralis (n=44), and Gl. sublingualis (n=30). All four salivary gland complexes showed allometric scaling with body mass (BM); in all cases, the 95% confidence interval for the allometric exponent included 0.75 but did not include 1.0 (linearity); therefore, like other parameters linked to the process of food intake, salivary gland mass appears to be correlated to metabolic body weight (BM0.75), and comparisons of relative salivary gland mass between species should rather be made on the basis of BM0.75 than as a percentage of BM. In the subsequent analyses, the percentage of grass (%grass) in the natural diet was used to characterize the feeding type; the phylogenetic tree used for a controlled statistical evaluation was entirely based on mitochondrial DNA information. Regardless of phylogenetic control in the statistical treatment, there was, for all four gland complexes, a significant positive correlation of BM and gland mass, and a significant negative correlation between %grass in the natural diet and gland mass. If the Gl. parotis was analyzed either for cervid or for bovid species only, the negative correlation of gland mass and %grass was still significant in either case; an inspection of certain ruminant subfamilies, however, suggested that a convergent evolutionary adaptation can only be demonstrated if a sufficient variety of ruminant subfamilies are included in a dataset. The results support the concept that ruminant species that ingest more grass have smaller salivary glands, possibly indicating a reduced requirement for the production of salivary tannin-binding proteins.     

Comparative omasum anatomy in ruminants: Relationships with natural diet,digestive physiology,and general considerations on allometric investigations

The omasum is the third forestomach compartment of pecoran ruminants. It is assumed that the re-absorption of fluid present in the forestomach digesta (that facilitates particle sorting, digestion, and harvest of microbes) is its main function, so that less diluted digesta is submitted to enzymatic digestion in the lower digestive tract. Here, we evaluate measures of omasum size (representing 84 ruminant species in the largest data set) against body mass and proxies of the natural diet (%grass) or forestomach physiology (fluid throughput), using phylogenetically controlled models. The origin of specimens (free-ranging or captive) did not have an effect in the data set. Models with the best support invariably either included %grass or a physiology proxy in addition to body mass. These effects were not necessarily additive (affecting the intercept of the allometric regression), but often indicated a change in the allometric body mass-exponent with diet or physiology. Only models that allowed an influence on the allometric exponent yielded basic exponents compatible with predictions derived from geometry. Species that include more grass in their natural diet, or that have a “cattle-type” physiology marked by a high forestomach fluid throughput, generally have larger omasa. However, the existence of outliers, as well as the overall data pattern, suggest that this is not an obligatory morphophysiological condition. Circumstantial evidence is presented leading to the hypothesis that the comparatively small and less complex omasa of “moose-type” species do not necessarily represent an “original” state, but may be derived from more complex states by ontogenetic reduction and fusion of omasal laminae.     

Sexual size dimorphism of the tongue in a North American pitviper

Sexual dimorphisms – phenotypic dissimilarities between the sexes – are common and widespread among plants and animals, and classical examples include differences in body size, colour, shape, ornamentation and behaviour. In general, sexual dimorphisms are hypothesized to evolve by way of sexual selection acting on one sex through priority-of-access for sexual partners via mate choice and/or intra-sexual competition. In snakes, males are the mate-searching sex and one form of sexual selection involves male–male competition in locating females by following pheromone trails using their forked tongues, the structure used to sample environmental chemicals for transduction in the vomeronasal chemosensory system (VNS). Based on several lines of empirical evidence, increased tongue forking (bifurcation) in snakes (and some lizard taxa) appears to enhance chemical trail-following abilities through tropotaxis (the simultaneous comparison of stimulus intensities on two sides of the body) and thus aids in prey location and mate searching in males. We predicted that male copperheads, Agkistrodon contortrix , a North American pitviper, should have more deeply forked tongues than females owing to male–male competition for priority-of-access to widely dispersed females during the mating seasons. We examined formalin-fixed, ethanol-preserved museum specimens of adult A. contortrix for sexual size dimorphism (SSD) of the tongue. Tongue dimensions showed differences indicative of SSD, and the degree of bifurcation (i.e. mean tine length) was significantly greater in males. Various structures of the VNS and associated regions (e.g. muscles) in some vertebrate taxa show sexual dimorphism, but our study is the first to document dimorphism in the tongue of a tetrapod vertebrate.     

Reanimation of the hemiparalytic tongue

Tongue hemiparesis is the inevitable result when the freshly severed 12th nerve is anastomosed to the trunk of a paralyzed 7th nerve in the technique commonly used by neurosurgeons, head and neck surgeons, otologists, and plastic surgeons to treat unilateral facial paralysis. This author has reactivated hemiparalytic tongues after research on cats. The technique has now been proved to be successful on two human beings. The reanimation is based on a simple Z-plasty of tongue muscle across the midline. Two principles are established: (1) placing a normal muscle in direct contact with a denervated muscle stimulates axons from the normal side to penetrate into the denervated side, eventually restoring function, and (2) transposition of a flap of muscle from the normal side containing extrinsic tongue muscles could provide a motor apparatus to activate the paralytic side. Biopsy slides taken from the paralyzed side of the cat tongues after 18 months showed sprouting of multiple nerves. Nerve sprouting can be found in human tongues 1 year after Z-plasties. The two patients who experienced atrophy and hemiparesis after the 12th-7th nerve hookup regained full range of tongue movements by 2 months and 4 months, respectively, demonstrating that with time, motor axons from the normal side innervated the atrophic muscle side to form new neuromotor junctions resulting in tongue movements. EMGs of the reanimated tongue showed normal activity in both sides of the tongue. Biopsies of the interface between the normal and former paralyzed side taken 1 year later showed nerves crossing the scar barrier. Apparently, the role of additional extrinsic muscle to the paralyzed side played a minor role.     

Butterfly nectaring flowers: butterfly morphology and flower form

The profitability of butterfly foraging depends in part on the corolla depth and clustering of flowers, and the tongue length, body mass and wing loading of butterflies. Interactions among these attributes of flowers and butterflies were investigated, using data from a field study in Cornwall and from Porter et al. (1992). The maximum corolla depth from which a butterfly can feed depends on tongue length, which correlates with the more easily measured attributes of body mass and wing loading. Small, short-tongued butterflies did not visit deep flowers. The quantity of nectar sugar per flower necessary for profitable foraging depends on foraging costs, which are expected to correlate with wing loading. Butterfly species with a high wing loading generally confined their visits to flowers that were clustered or very nectar-rich. Butterfly species with a low wing loading included solitary and less nectar-rich flowers in their diet. Body mass and wing loading affect a butterfly's load-carrying capacity (limiting the distance between fuelling stops) and cooling rate (limiting the distance between stops for basking or endothermic warming), and will therefore influence the capacity for floral selectivity and for migration and dispersal. Body mass, wing loading and tongue length characterised families or subfamilies of butterflies. For example vanessine nymphalids, with their long tongues and high wing loading, visited the deep, massed flowers of Buddleja davidii, but lycaenids, with their short tongues and low wing loading, did not. These often visited members of the Asteraceae. Eupatorium cannabinum, with massed flowers offering abundant and accessible nectar, was visited by butterflies of all tongue lengths and both high and low wing loading. These findings may help to inform habitat management for butterfly nectaring flowers.     

Assessment of cell proliferation and muscular structure following surgical tongue volume reduction in pigs

Objectives: Tongue volume reduction is an adjunct treatment in several orofacial orthopaedic procedures for various craniofacial deformities; it may affect structural reconstitution and functional recovery as a result of the repair process. The aim of this study was to investigate myogenic regeneration and structural alteration of the tongue following surgical tongue volume reduction. Materials and methods: Five 12‐week‐old sibling pairs of Yucatan minipigs (three males and two females) were used. Midline uniform glossectomy was performed on one of each pair (reduction); siblings had identical incisions without tissue removal (sham). All pigs were raised for a further 4 weeks and received 5‐bromo‐2‐deoxyuridine (BrdU) injection intravenously 1 day before killing. Tissue sections of tongues were stained with anti‐BrdU antibody to evaluate numbers of replicating cells. Haematoxylin and eosin plus trichrome staining were performed to assess muscular structure. Results: Reduction tongues contained significantly more BrdU+ cells compared to sham tongues (P < 0.01). However, these BrdU+ cells were mostly identified in reparative connective tissues (fibroblasts) rather than in regenerating muscle tissue (myoblasts). Trichrome‐stained sections showed disorganized collagen fibres linked to few intermittent muscle fibres in the reduction tongues. These myofibres presented signs of atrophy with reduced perimysium and endomysium. Matrix between reduced perimysium and endomysium was filled with fibrous tissue. Conclusions: Fibrosis without predominant myogenic regeneration was the major histological consequence of surgical tongue volume reduction.     

Brief communication: Noninvasive measuring of operational tongue length in callitrichids

Callitrichids use their tongue in various social, ecological, and hygienic contexts. Using a noninvasive measuring device, we obtained data on the operational tongue length (OTL) in seven species from the family Callitrichidae. OTL (defined as the maximum tongue extension into the device) varied significantly between species and the width of the device, but did not correlate with mandible length; it is smaller in relation to mandible length in Leontopithecus chrysomelas compared to species from the genera Saguinus and Callithrix. Current information does not allow concluding which of the various functions of the tongue is selecting for tongue length. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Review of the evolution and phylogeny of the mammalian tongue.

Evolution of the mammalian tongue has been characterized by a number of extensive structural adaptations for the highly specialized functions which various tongues perform. Variations in shape, epithelium, muscle arrangement and mechanisms of lingual stiffening are described, and the possible way in which such changes have occurred is discussed. The review also shows that a study of the tongue's structure in conjunction with other anatomical features may serve as a useful indicator of an animal's habits and diet and provide important information for taxonomic purpose.     

Filiform papillae of human, rat and swine tongue

In order to study the structure of filiform papillae (FP), tissue specimens were taken from the anterior part of the tongues of 8 humans, 8 rats and 8 swine. The formalin-fixed samples were processed routinely for scanning electron microscopy (SEM) and light microscopy. With SEM, FP of human tongue contained 5-12 hairs which were covered with a massive plaque of micro-organisms. FP of rat tongue, on the other hand, contained one papillary projection with smooth surface structure. Colonization of micro-organisms was seen on the anterior part of the body of FP, but not on the hairs. In the cross-section of FP of the rat tongue, the cells of the papilla were close to each other and no micro-organisms were seen within the papillae. On the contrary, the spaces between the squamous epithelial cells of the hairs of human FP contained numerous micro-organisms. The structure of FP of the swine tongue resembled that of the rat tongue. The hairs were smooth, and some micro-organisms were seen on the cell surface of the interpapillary areas. The structure of FP is discussed from the standpoint of different keratinization and colonization of micro-organisms.     

Anatomy of the tongue and microstructure of the lingual papillae in the fallow deer Dama dama (Linnaeus, 1758)

The function of mouth organs in ruminants is connected with the process of rumination. To study morphofunctional relations, microstructures in tongues of 4- to 5-year old adult fallow deer were examined using scanning electron microscopy.When analyzing the tongue of the fallow deer, i.e. a ruminant classified as an intermediate mixed feeder between grass and roughage eaters, two processes were taken into account: (i) foraging and forage selecting, and (ii) chewing the cud during rumination to reduce particle size and improve digestibility.Microstructural results show that the above mentioned processes in fallow deer are important selection factors, which in the anterior part of tongue led to the development of clusters of fungiform papillae connected with preselection of food as well as a specific pattern of filiform papillae promoting increased adhesion of transported food. Massive and flattened conical papillae on the torus are arranged according to sideways jaw movements and are co-localized with flattened fungiform papillae and two rows of vallate papillae. Such an arrangement of papillae on the lingual torus presumably facilities distribution of ruminated food, with simultaneous transferring of taste signals about masticated food particles.     

Comparison of isometric contractile properties of the tongue muscles in three species of frogs, Litoria caerulea, Dyscophus guinetti, and Bufo marinus.

Previous studies show that anurans feed in at least three different ways. Basal frogs have a broad tongue that shortens during protraction and emerges only a short distance from the mouth. Some frogs have long, narrow tongues that elongate dramatically due primarily to inertia from mouth opening, which is transferred to the tongue. A few species have a hydrostatic mechanism that produces tongue elongation during protraction. This functional diversity occurs among frogs that share the same two pairs of tongue muscles. Our study compares the isometric contractile properties of these tongue muscles among three frog species that represent each feeding mechanism. Nerves to the paired protractors and retractors were stimulated electrically in each species to record the force properties, contraction speeds, and fatigabilites of these muscles. Few differences were found in the isometric contractile properties of tongue muscles, and the greatest differences were found in the retractors, not the protractors. We propose that the unique arrangement of the tongue muscles in frogs results in a retractor that may also be coactivated with the protractor in order to produce normal tongue protraction. Inertial effects from body, head, and jaw movements, along with clear differences that we found in passive resistance of the tongues to elongation, may explain much of the behavioral variation in tongue use among species.     

Manipulators inspired by the tongue of the chameleon

Chameleons have developed a specialized ballistic tongue which elongates more than six times its rest length at speeds higher than 3.5 m s(-1) and accelerations 350 m s(-2), with a highly flexible mobile part, and which applies no continuous force during forward motion. These characteristics are possible because this tongue consists of two highly specialized systems, an ejection system for the forward motion and an accordion-like system for the retraction. Four manipulators inspired by the tongue of the chameleon and based on this design have been developed, resulting in three characteristics similar to the tongue of the chameleon: extensibility of the manipulator, flexibility of the mobile part, and absence of continuous force during the forward motion. The first manipulator mimics the basic mechanism of the tongue of the chameleon and reproduced its basic performances. A second manipulator performs a catching function at a speed of 3.5 m s(-1) with an acceleration of 573 m s(-2) while elongating seven times its rest length. The design of this manipulator is such that the dc motor used for retraction applies a torque 25 times its rated torque. Moreover, during the retraction, the mobile part of the manipulator moves due to its own inertia, allowing the dc motor to rotate at full velocity. In another manipulator, the addition of an elastomer in the mobile part allows for control of the retraction velocity. A model for these two manipulators compares well with the experimental data. Finally, the addition of wings on the mobile part allows us to take the advantage of aerodynamic effects, which is unusual for manipulators.     

Comparative anatomic studies of the tongue of Pan troglodytes (Blumenbach, 1799) and other primates. I. The chimpanzee tongue

This study was carried out on a comprehensive collection of tongues of Pan troglodytes. Material of tongues of Tupaia glis, Microcebus murinus, Chirogaleus major, Lemur catta, Galago crassicaudatus, Cebus apella, and Macaca mulatta were used for comparison of the different stages of the development of the papilla foliata. The tongue of Pan exhibits longitudinal growth correlated with the growth of length of the jaws and individual age. A typical foramen caecum as it occurs in man was gross anatomically not recognizable. Seldom a small circular depression appeared in the midline close to the papilla circumvallata centralis which could be the remnant of the foramen caecum. There is a remarkable accumulation of papillae filiformes and fungiformes at the apex linguae; the same seems to be true for other genera of primates. It is self-explanatory that the accumulation of papillae makes the tip of the tongue a particularly sensitive area; this has been found to be true even in man. One specimen of the prenatal age just before term was studied. It exhibited remarkably elongated, thread-like papillae, their function is unknown as yet. They are no longer present in a newborn specimen of 4 d of age. In the aboral part of the dorsum linguae, a special kind of papillae occur; they are flat lobes which carry moderately elongated, tiny processes at their free margin. The function of these papillae is unknown; taste buds are absent.     

Embryogenesis of the human tongue]

Developmental peculiarities of the tongue as a whole and its main structural elements (muscles, membranes, glands, lingual tonsil) have been studied in 120 human embryos and fetuses 5-week-old--9-month-old. Transmissive electron microscopy, electron histochemistry (for estimation of 5'-nucleotidase activity), staining of semithin slices with toluidine blue and aniline++ pink have been applied. Problems on migration of myogenic elements in the developing tongue have been discussed. Ultrastructure of gustatory bulbs of the human fetus tongues has been investigated. A complete formation of the tongue takes place by the 8th-9th months of the prenatal development.     

Rapid prion neuroinvasion following tongue infection

Food-borne transmission of prions can lead to infection of the gastrointestinal tract and neuroinvasion via the splanchnic and vagus nerves. Here we report that the transmission of transmissible mink encephalopathy (TME) is 100,000-fold more efficient by inoculation of prions into the tongues of hamsters than by oral ingestion. The incubation period following TME agent (hereinafter referred to as TME) inoculation into the lingual muscles was the shortest among the five nonneuronal routes of inoculation, including another intramuscular route. Deposition of the abnormal isoform of the prion protein, PrP(Sc), was first detected in the tongue and submandibular lymph node at 1 to 2 weeks following inoculation of the tongue with TME. PrP(Sc) deposits in the tongue were associated with individual axons, and the initial appearance of TME in the brain stem was found in the hypoglossal nucleus at 2 weeks postinfection. At later time points, PrP(Sc) was localized to brain cell groups that directly project to the hypoglossal nucleus, indicating the transneuronal spread of TME. TME PrP(Sc) entry into the brain stem preceded PrP(Sc) detection in the rostral cervical spinal cord. These results demonstrate that TME can replicate in both the tongue and regional lymph nodes but indicate that the faster route of brain invasion is via retrograde axonal transport within the hypoglossal nerve to the hypoglossal nucleus. Topical application of TME to a superficial wound on the surface of the tongue resulted in a higher incidence of disease and a shorter incubation period than with oral TME ingestion. Therefore, abrasions of the tongue in livestock and humans may predispose a host to oral prion infection of the tongue-associated cranial nerves. In a related study, PrP(Sc) was detected in tongues following the intracerebral inoculation of six hamster-adapted prion strains, which demonstrates that prions can also travel from the brain to the tongue in the anterograde direction along the tongue-associated cranial nerves. These findings suggest that food products containing ruminant or cervid tongue may be a potential source of prion infection for humans.     

Resource competition triggers the co-evolution of long tongues and deep corolla tubes

Background

It is normally thought that deep corolla tubes evolve when a plant''s successful reproduction is contingent on having a corolla tube longer than the tongue of the flower''s pollinators, and that pollinators evolve ever-longer tongues because individuals with longer tongues can obtain more nectar from flowers. A recent model shows that, in the presence of pollinators with long and short tongues that experience resource competition, coexisting plant species can diverge in corolla-tube depth, because this increases the proportion of pollen grains that lands on co-specific flowers.

Methodology/Principal Findings

We have extended the model to study whether resource competition can trigger the co-evolution of tongue length and corolla-tube depth. Starting with two plant and two pollinator species, all of them having the same distribution of tongue length or corolla-tube depth, we show that variability in corolla-tube depth leads to divergence in tongue length, provided that increasing tongue length is not equally costly for both species. Once the two pollinator species differ in tongue length, divergence in corolla-tube depth between the two plant species ensues.

Conclusions/Significance

Co-evolution between tongue length and corolla-tube depth is a robust outcome of the model, obtained for a wide range of parameter values, but it requires that tongue elongation is substantially easier for one pollinator species than for the other, that pollinators follow a near-optimal foraging strategy, that pollinators experience competition for resources and that plants experience pollination limitation.     

Gross anatomical features of the tongue, lingual skeleton and laryngeal mound of Rhea americana (Palaeognathae, Aves): morpho-functional considerations

The tongue body of Rhea americana is triangular and partially pigmented with each caudo-lateral margin displaying a round, sub-divided lingual papilla. The tongue root is a smooth, non-pigmented tract of mucosa. The tongue body is supported by the paraglossum and distal half of the rostral projection of the basihyal (RPB), and the tongue root by the proximal half of the RPB, body of the basihyal and proximal ceratobranchials. An urohyal is absent; however, peculiar to R. americana, the caudal margin of the cricoid body displays a median projection, which may represent the remnant of the urohyal incorporated into the cricoid. The laryngeal mound is less elevated, the arytenoid cartilages are smaller than in other ratites, and the caudal margin displays pharyngeal papillae that vary in shape and number. The unique morphology of the lingual skeleton and its positioning within the tongue of R. americana, the rostral insertion of the M. ceratoglossus, the absence of the urohyal (enhanced ventroflexion) and the caudal positioning and mobile attachment of the ensheathed basihyal to the paraglossum would appear to allow independent movement of the tongue body relative to the hyobranchial apparatus. Additionally, the deeply indented base and rostral oval opening in the paraglossum limits the length of cartilage present in the midline of the tongue body. This may allow the tongue the necessary flexibility for the lingual papillae to clean the choana. The cleaning action of the tongue would occur simultaneously with the previously described role of this organ and associated structures during feeding. Thus, the so-called reduced, ancestral tongue of R. americana may be structurally and functionally more complex than previously believed.