A fish that uses its hydrodynamic tongue to feed on land

To capture and swallow food on land, a sticky tongue supported by the hyoid and gill arch skeleton has evolved in land vertebrates from aquatic ancestors that used mouth-cavity-expanding actions of the hyoid to suck food into the mouth. However, the evolutionary pathway bridging this drastic shift in feeding mechanism and associated hyoid motions remains unknown. Modern fish that feed on land may help to unravel the physical constraints and biomechanical solutions that led to terrestrialization of fish-feeding systems. Here, we show that the mudskipper emerges onto land with its mouth cavity filled with water, which it uses as a protruding and retracting ‘hydrodynamic tongue’ during the initial capture and subsequent intra-oral transport of food. Our analyses link this hydrodynamic action of the intra-oral water to a sequence of compressive and expansive cranial motions that diverge from the general pattern known for suction feeding in fishes. However, the hyoid motion pattern showed a remarkable resemblance to newts during tongue prehension. Consequently, although alternative scenarios cannot be excluded, hydrodynamic tongue usage may be a transitional step onto which the evolution of adhesive mucosa and intrinsic lingual muscles can be added to gain further independence from water for terrestrial foraging.     

Light and transmission electron microscopy of the dorsal lingual epithelium of Pelusios castaneus (Pleurodira, Chelidae) with special respect to its feeding mechanics

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.     

Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi)

The feeding mechanism of the South American lungfish, Lepidosiren paradoxa retains many primitive teleostome characteristics. In particular, the process of initial prey capture shares four salient functional features with other primitive vertebrates: 1) prey capture by suction feeding, 2) cranial elevation at the cranio-vertebral joint during the mouth opening phase of the strike, 3) the hyoid apparatus plays a major role in mediating expansion of the oral cavity and is one biomechanical pathway involved in depressing the mandible, and 4) peak hyoid excursion occurs after maximum gape is achieved. Lepidosiren also possesses four key morphological and functional specializations of the feeding mechanism: 1) tooth plates, 2) an enlarged cranial rib serving as a site for the origin of muscles depressing the hyoid apparatus, 3) a depressor mandibulae muscle, apparently not homologous to that of amphibians, and 4) a complex sequence of manipulation and chewing of prey in the oral cavity prior to swallowing. The depressor mandibulae is always active during mouth opening, in contrast to some previous suggestions. Chewing cycles include alternating adduction and transport phases. Between each adduction, food may be transported in or out of the buccal cavity to position it between the tooth plates. The depressor mandibulae muscle is active in a double-burst pattern during chewing, with the larger second burst serving to open the mouth during prey transport. Swallowing is characterized by prolonged activity in the hyoid constrictor musculature and the geniothoracicus. Lepidosiren uses hydraulic transport achieved by movements of the hyoid apparatus to position prey within the oral cavity. This function is analogous to that of the tongue in many tetrapods.     

Aquatic feeding in a terrestrial turtle: a functional-morphological study of the feeding apparatus in the Indochinese box turtle Cuora galbinifrons (Testudines, Geoemydidae)

The Indochinese box turtle Cuora galbinifrons is regarded as a purely terrestrial species, but our results demonstrate that it can feed both on land and in water. The inverse relationship between the relative development of the hyoid apparatus and the tongue found in the most investigated chelonians is not valid in the Indochinese box turtle. Our morphological analysis of the feeding apparatus reveals that the palate shape and the design of the tongue are consistent with terrestrial feeders, but the construction of the hyoid complex is more characteristic of aquatic feeders. Previous studies have demonstrated that tongue enlargement negatively impacts the capacity of the turtles to suction feed. The present study focuses on the aquatic intraoral prey transport kinematic patterns. Our analysis is based on high-speed films with 250 fr/s and high-speed cineradiography with 50 fr/s. The aquatic intraoral food transport mechanisms differ depending on prey size: small items are transported predominantly by “inertial suction”, whereas larger items are moved by the tongue—normally a clear terrestrial strategy. As the genus Cuora is ancestrally aquatic, the use of lingual food transport in the aquatic environment is presumably an aberrant modus typical only for the most terrestrial among the Asian box turtles.     

Comparative anatomy and evolutionary history of suction feeding in cetaceans

Some odontocetes possess unique features of the hyolingual apparatus that are involved in suction feeding. The hyoid bone and associated musculature generates rapid, piston‐like retraction, and depression of the hyoid and tongue. “Capture” suction feeders (e.g., Globicephala) use suction for capturing and swallowing prey. “Combination” feeders (i.e., Lagenorhynchus) use both raptorial feeding (to capture prey) and suction (to ingest prey). In “capture” suction feeders, features of the hyoid and skull have been attributed to creating suction (i.e., large surface area and mandibular bluntness). In addition to odontocetes, a mysticete, the gray whale (Eschrichtius robustus), is considered a benthic suction feeder. However, anatomical studies of purported suction‐feeding structures of the gray whale are lacking. In addition, few studies have utilized evolutionary approaches to understand the history of suction feeding in cetaceans. This study incorporates quantitative and qualitative hyoid and cranial data from 35 extant and 14 extinct cetacean species into a multivariate principal component analysis and comparative phylogenetic analyses. Conclusions from these analyses are that some commonly attributed features (i.e., ventral throat grooves and mandibular bluntness) and one principal component are significantly correlated with suction feeding. Finally, ancestral state reconstructions indicate that suction feeding likely evolved once, early in cetacean evolutionary history.     

Oropharyngeal morphology in the basal tortoise Manouria emys emys with comments on form and function of the testudinid tongue

In tetrapods, the ability to ingest food on land is based on certain morphological features of the oropharynx in general and the feeding apparatus in particular. Recent paleoecological studies imply that terrestrial feeding has evolved secondarily in turtles, so they had to meet the morphological oropharyngeal requirements independently to other amniotes. This study is designed to improve our limited knowledge about the oropharyngeal morphology of tortoises by analyzing in detail the oropharynx in Manouria emys emys. Special emphasis is placed on the form and function of the tongue. Even if Manouria is considered a basal member of the only terrestrial turtle clade and was hypothesized to have retained some features reflecting an aquatic ancestry, Manouria shows oropharyngeal characteristics found in more derived testudinids. Accordingly, the oropharyngeal cavity in Manouria is richly structured and the glands are large and complexly organized. The tongue is large and fleshy and bears numerous slender papillae lacking lingual muscles. The hyolingual skeleton is mainly cartilaginous, and the enlarged anterior elements support the tongue and provide insertion sides for the well‐developed lingual muscles, which show striking differences to other reptiles. We conclude that the oropharyngeal design in Manouria differs clearly from semiaquatic and aquatic turtles, as well as from other reptilian sauropsids. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

The ontogeny of functional design: metamorphosis of feeding behaviour in the tiger salamander (Ambystoma tigrinum)

The ontogeny of feeding behaviour was studied quantitatively in the tiger salamander, Ambystoma tigrinum , to elucidate the relative importance of morphological and environmental changes on form and function. High-speed films of prey capture provided data for a frame-by-frame analysis of seven kinematic parameters of feeding behaviour. By comparing underwater feeding of larval and metamorphosed individuals, the effect of morphological changes occurring at metamorphosis on the feeding kinematic pattern was determined. By comparing metamorphosed animals feeding in the water and on land, changes in feeding kinematics associated with the environmental transition (and thus the differing physical properties of water and air) were determined. Both univariate and multivariate analyses failed to demonstrate any differences between larval and metamorphosed aquatic feedings for seven kinematic variables. However, when individuals feed on land, a radical shift in hyoid kinematics was observed. In addition, multivariate analysis showed that terrestrial feedings differed from aquatic feedings in having longer duration head movements. The lack of a kinematic difference between larval and metamorphosed individuals feeding in the water indicates that the morphological changes occurring at metamorphosis do not impose any obligatory kinematic consequences. Rather, metamorphosed Ambystoma tigrinum acquire the ability to modulate their kinematic pattern depending on the environment.     

Kinematics of the jaw and hyolingual apparatus during feeding in Caiman crocodilus

Movements of the neck, jaws, and hyolingual apparatus during inertial feeding in Caiman crocodilus were studied by cineradiography. Analysis reveals two kinds of cycles: inertial bites (reposition, kill/crush, and transport) and swallowing cycles. They differ in their gape profile and in displacement of the neck, cranium, and hyolingual apparatus. Inertial bites are initiated by an elevation of the neck and cranium; the head is then retracted backward, the prey simultaneously being lifted by the hyolingual apparatus. Next the lower jaw is depressed, and the prey is rapidly pushed further upward by the hyolingual apparatus. Thereafter fast mouth-closure occurs with the neck and cranium being abruptly depressed, the lower jaw elevated, and the hyolingual apparatus rapidly retracted ventrally. Depression of the neck and cranium thrusts the head forward and impacts the backward moving prey more posteriorly in the oral cavity. Swallowing cycles initially involve movement of the hyoid in front of the prey followed by rapid posteroventrad retraction of the hyoid, forcing the prey into the esophagus during opening and closing of the mouth. After mouth-closure, the hyoid apparatus is again protracted. Jaws, neck, tongue, and hyoid apparatus play an active role during intertial feeding sequences. At the beginning of a feeding sequence, the hyolingual apparatus mainly moves dorsoventrally, whereas toward the end of a sequence anteroposterior displacements of the hyoid are prominent. © 1992 Wiley-Liss, Inc.     

Prey processing in the Siamese fighting fish (Betta splendens)

We studied prey processing in the Siamese fighting fish (Betta splendens), involving slow, easily observed head-bobbing movements, which were compared with prey processing in other aquatic feeding vertebrates. We hypothesized that head-bobbing is a unique prey-processing behaviour, which alternatively could be structurally and functionally analogous with raking in basal teleosts, or with pharyngognathy in neoteleosts. Modulation of head-bobbing was elicited by prey with different motility and toughness. Head-bobbing involved sustained mouth occlusion and pronounced cranial elevation, similar to raking. However, the hyoid and pectoral girdle were protracted, and not retracted as in both raking and pharyngognathy. High-speed videofluoroscopy of hyoid movements confirmed that head-bobbing differs from other known aquatic prey-processing behaviours. Nevertheless, head-bobbing and other prey-processing behaviours converge on a recurrent functional theme in the trophic ecology of aquatic feeding vertebrates; the use of intraoral and oropharyngeal dentition surfaces to immobilize, reduce and process relatively large, tough or motile prey. Prey processing outside the pharyngeal region has not been described for neoteleosts previously, but morphological evidence suggests that relatives of Betta might use similar processing behaviours. Thus, our results suggest that pharyngognathy did not out-compete ancestral prey-processing mechanisms completely during the evolution of neoteleosts.     

The use of the tongue and hyoid apparatus during feeding in lizards (Ctenosaura similis and Tupinambis nigropunctatus)

The use of the tongue and hyoid is examined in cineradiographic and electromyographic investigations of feeding in two species of lizards, Ctenosaura similis (Iguanidae) and Tupinambis nigropunctatus (Teiidae). In both animals food is transported through the oral cavity by regular cycles of the tongue. Tongue movements correlate with jaw and hyoid movement. Similarities between the two animals in the use of the tongue in food transport, lapping, pharyngeal packing, and pharyngeal emptying are detailed. Mechanisms of tongue protrusion are examined and it is shown that the tongue in Tupinambis is relatively more protrusible than in Ctenosaura. This difference is complementary with data on the greater reliance of Tupinambis on the tongue as a sensory organ. Tupinambis further differs from Ctenosaura in possessing a greater mobility of the hyoid. In many features of tongue use in food transport, lizards resemble mammals, supporting postulations of a basic pattern of intra-oral food transport. However, whether this pattern can be attributed to convergence or a common, primitive neural pattern of control cannot be distinguished. Lizards lack two major characteristics of mammalian food transport: regular masticatory cycles and an internal swallowing mechanism.     

Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type

The ability to modulate feeding kinematics in response to prey items with different functional properties is likely a prerequisite for most organisms that feed on a variety of food items. Variation in prey properties is expected to reveal variation in feeding function and the functional role of the different phases in a transport cycle. Here we describe the kinematics of prey transport of two varanid species, Varanus niloticus and Varanus ornatus. These species were selected for analysis because of their highly specialised hyolingual system and food transport mechanism (inertial food transport). In these animals, tongue and hyoid movements are expected to make no, or only a minor, contribution to prey transport. We observed statistically significant prey type effects that could be associated with prey properties such as mass, size and mobility. These data show that both species are capable of modulating the kinematics of food transport in response to different prey types. Moreover, not only the kinematics of the jaws were modulated in response to prey characteristics but also the anterior/posterior movements of the tongue and hyoid. This suggests a more important role of the tongue and hyolingual movements in these animals than previously suspected. In contrast, head movements were rather stereotyped and were not modulated in response to changes in prey type.     

The suction mechanism of the pipid frog,Pipa pipa (Linnaeus, 1758)

Most suction‐feeding, aquatic vertebrates create suction by rapidly enlarging the oral cavity and pharynx. Forceful enlargement of the pharynx is powered by longitudinal muscles that retract skeletal elements of the hyoid, more caudal branchial arches, and, in many fish, the pectoral girdle. This arrangement was thought to characterize all suction‐feeding vertebrates. However, it does not exist in the permanently aquatic, tongueless Pipa pipa , an Amazonian frog that can catch fish. Correlating high‐speed (250 and 500 fps) video records with anatomical analysis and functional tests shows that fundamental features of tetrapod body design are altered to allow P. pipa to suction‐feed. In P. pipa , the hyoid apparatus is not connected to the skull and is enclosed by the pectoral girdle. The major retractor of the hyoid apparatus arises not from the pectoral girdle but from the femur, which lies largely within the soft tissue boundaries of the trunk. Retraction of the hyoid is coupled with expansion of the anterior trunk, which occurs when the hypertrophied ventral pectoral elements are depressed and the urostyle and sacral vertebra are protracted and slide forward on the pelvic girdle, thereby elongating the entire trunk. We suggest that a single, robust pair of muscles adduct the cleithra to depress the ventral pectoral elements with force, while modified tail muscles slide the axial skeleton cranially on the pelvic girdle. Combined hyoid retraction, axial protraction, and pectoral depression expand the buccopharyngeal cavity to a volume potentially equal to that of the entire resting body of the frog. Pipa may be the only tetrapod vertebrate clade that enlarges its entire trunk during suction‐feeding.     

Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders

This study addresses four questions in vertebrate functional morphology through a study of aquatic prey capture in ambystomatid salamanders: (1) How does the feeding mechanism of aquatic salamanders function as a biomechanical system? (2) How similar are the biomechanics of suction feeding in aquatic salamanders and ray-finned fishes? (3) What quantitative relationship does information extracted from electromyograms of striated muscles bear to kinematic patterns and animal performance? and (4) What are the major structural and functional patterns in the evolution of the lower vertebrate skull? During prey capture, larval ambystomatid salamanders display a kinematic pattern similar to that of other lower vertebrates, with peak gape occurring prior to both peak hyoid depression and peak cranial elevation. The depressor mandibulae, rectus cervicis, epaxialis, hypaxialis, and branchiohyoideus muscles are all active for 40–60 msec during the strike and overlap considerably in activity. The two divisions of the adductor mandibulae are active in a continuous burst for 110–130 msec, and the intermandibularis posterior and coracomandibularis are active in a double burst pattern. The antagonistic depressor mandibulae and adductor mandibulae internus become active within 0.2 msec of each other, but the two muscles show very different spike and amplitude patterns during their respective activity periods. Coefficients of variation for kinematic and most electromyographic recordings reach a minimum within a 10 msec time period, just after the mouth starts to open. Pressure within the buccal cavity during the strike reaches a minimum of ?25 mmHg, and minimum pressure occurs synchronously with maximum gill bar adduction. The gill bars (bearing gill rakers that interlock with rakers of adjacent arches) clearly function as a resistance within the oral cavity and restrict posterior water influx during mouth opening, creating a unidirectional flow during feeding. Durations of electromyographic activity alone are poor predictors of kinematic patterns. Analyses of spike amplitude explain an additional fraction of the variance in jaw kinematics, whereas the product of spike number and amplitude is the best statistical predictor of kinematic response variables. Larval ambystomatid salamanders retain the two primitive biomechanical systems for opening and closing the mouth present in nontetrapod vertebrates: elevation of the head by the epaxialis and depression of the mandible by the hyoid apparatus.     

Functional morphology of the feeding apparatus,feeding constraints,and suction performance in the nurse shark Ginglymostoma cirratum

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction‐feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction‐feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior‐directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic‐feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction‐feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Functional morphology of the head of the anabantoid teleost fish Helostoma temmincki

Osteology, myology and motion analysis of the head of the anabantoid fish Helostoma temmincki, a specialized filter feeder, has revealed six functional units: neurocranium, suspensory apparatus, opercular apparatus, hyoid apparatus, branchial apparatus and pectoral girdle. Interactions between the functional units take place through four couplings involved in opening and protruding the jaws. The first coupling is activated in the beginning of the opening cycle by the levator operculi muscle through the opercular apparatus, interoperculomandibular ligament and mandible. The second is activated during feeding by contraction of the sternohyoideus through the hyoid apparatus, interopercular, interoperculomandibular ligament and mandible. The third coupling is active during feeding and “kissing” by contraction of epaxial muscles through mediation of the neurocranium to the jaw apparatus. The fourth coupling is the only one active during air intake and involves contraction of the levator arcus palatini which abducts and rotates the suspensory apparatus forwards, causing the mandible to drop. The retention of isolated ancestral characters during mosaic evolution are explained in terms of the maintenance of couplings which represent functional associations of seemingly remote structures. When natural selection acts on one component of a functional unit or coupling, it essentially acts on all associated elements simultaneously causing character complexes to evolve in common evolutionary trends. It is feasible that functional analysis can separate primary from secondary evolutionary trends.     

Movement of the hyoid in frogs during feeding.

Feeding, breathing, and vocalization sequences of Bufo marinus were recorded by cineradiography. Results of film analysis indicate that the hyoid moves during all three behaviors. Movement of the hyoid is critical in tongue protrusion of frogs, and a biomechanical model of this action is presented. The hyoid appears to represent a compromise morphological system for three functions, rather than an optimal system for any one. This may explain, in part, the retention of a relatively inefficient breathing mechanism in frogs.     

Adaptations of the hoatzin (Opisthocomus hoazin) to leaf-eating. Morphological characteristics and functional features of its bill and hyoid apparatus

The hoatzin remains one of the most enigmatic birds. A morphofunctional analysis of its bill and hyoid apparatus throws new light on its feeding adaptation as well as on its systematic relationships. Bony and muscular skull, rhamphotheca, palate, and hyoid apparatus were described in details. Though keeping into the general organisation pattern found among Neognathae (except Galliformes), bill and hyoid apparatus of the hoatzin displays a series of species-specific features, some unique among birds. This species appears particularly well adapted to tear of leaves and process them inside the bill before ingestion. Because of very important anatomical and thence functional differences in bill and hyoid structure, any close relationship between the hoatzin and Galliformes cannot be envisioned. Such a hypothesis would implicate a counter-selective evolutionary reversion.     

Analysis of prey capture and food transport kinematics in two Asian box turtles,Cuora amboinensis and Cuora flavomarginata (Chelonia,Geoemydidae), with emphasis on terrestrial feeding patterns

This study examines the kinematics and morphology of the feeding apparatus of two geoemydid chelonians, the Malayan (Amboina) box turtle (Cuora amboinensis) and the yellow-margined box turtle (Cuora flavomarginata). Both species are able to feed on land as well as in water. Feeding patterns were analysed by high-speed cinematography. The main focus of the present study is on the terrestrial feeding strategies in both Asian box turtles, because feeding on land has probably evolved de novo within the ancestrally aquatic genus Cuora. During terrestrial feeding (analysed for both species), the initial food prehension is always done by the jaws, whereas intraoral food transport and pharyngeal packing actions are tongue-based. The food uptake modes in Cuoras differ considerably from those described for purely terrestrial turtles. Lingual food prehension is typical of all tortoises (Testudinidae), but is absent in C. amboinensis and C. flavomarginata. A previous study on Terrapene carolina shows that this emydid turtle protrudes the tongue during ingestion on land, but that the first contact with the food item occurs by the jaws. Both Asian box turtles investigated here have highly movable, fleshy tongues; nonetheless, the hyolingual complex remains permanently retracted during initial prey capture. In aquatic feeding (analysed for C. amboinensis only), the prey is captured by a fast forward strike of the head (ram feeding). As opposed to ingestion on land, in the underwater grasp the hyoid protracts prior to jaw opening. The head morphology of the investigated species differs. In contrast to the Malayan box turtle, C. flavomarginata exhibits a more complexly structured dorsal lingual epithelium, a considerable palatal vault, weaker jaw adductor muscles and a simplified trochlear complex. The differences in the hyolingual morphology reflect the kinematic patterns of the terrestrial feeding transport.