Buccal Pump Research Articles

Onset of buccal pumping in catshark embryos: how breathing develops in the egg capsule.

Respiration in fishes involves buccal pumping, which is characterized by the generation of nearly continuous water flow over the gills because of the rhythmic expansion/compression of the pharyngeal cavity. This mechanism is achieved by the functions of the vascular, skeletal, and muscular systems. However, the process by which the embryo establishes the mechanism remains a mystery. Morphological and kinematical observations on captive cloudy catsharks, Scyliorhinus torazame, have suggested that the embryo starts buccal pumping just before the respiratory slits open on the egg capsule. During the pre-opening period, the embryo acquires oxygen mainly via the external gill filaments. After slit opening, respiration of the embryo involves buccal pumping to pass water over the “internal gills.” The onset of buccal pumping accompanies four morphological changes: (1) regression of the external gill filaments, (2) development of blood vessels within the “internal gills,” (3) completion of the development of hyoid skeletal and muscular elements, and (4) development of the oral valve. A previous study showed that buccal pumping allows the embryo to actively regulate oxygen intake by changing the pumping frequency. Thus, establishment of buccal pumping in the egg capsule is probably important for embryo survival in the unstable oxygen environment of the egg capsule after slit opening.

An exceptionally preserved transitional lungfish from the lower permian of Nebraska, USA, and the origin of modern lungfishes.

Complete, exceptionally-preserved skulls of the Permian lungfish Persephonichthys chthonica gen. et sp. nov. are described. Persephonichthys chthonica is unique among post-Devonian lungfishes in preserving portions of the neurocranium, permitting description of the braincase of a stem-ceratodontiform for the first time. The completeness of P. chthonica permits robust phylogenetic analysis of the relationships of the extant lungfish lineage within the Devonian lungfish diversification for the first time. New analyses of the relationships of this new species within two published matrices using both maximum parsimony and Bayesian inference robustly place P. chthonica and modern lungfishes within dipterid-grade dipnoans rather than within a clade containing Late Devonian ‘phaneropleurids’ and common Late Paleozoic lungfishes such as Sagenodus. Monophyly of post-Devonian lungfishes is not supported and the Carboniferous-Permian taxon Sagenodus is found to be incidental to the origins of modern lungfishes, suggesting widespread convergence in Late Paleozoic lungfishes. Morphology of the skull, hyoid arch, and pectoral girdle suggests a deviation in feeding mechanics from that of Devonian lungfishes towards the more dynamic gape cycle and more effective buccal pumping seen in modern lungfishes. Similar anatomy observed previously in ‘Rhinodipterus’ kimberyensis likely represents an intermediate state between the strict durophagy observed in most Devonian lungfishes and the more dynamic buccal pump seen in Persephonichthys and modern lungfishes, rather than adaptation to air-breathing exclusively.

Lamprey breathing when feeding sucks: the respiratory rhythm generator of a parasitic fish.

Lamprey breathing when feeding sucks: the respiratory rhythm generator of a parasitic fish.

Fiber‐type composition in the perivertebral musculature of lizards: Implications for the evolution of the diapsid trunk muscles

The perivertebral musculature of lizards is critical for the stabilization and the mobilization of the trunk during locomotion. Some trunk muscles are also involved in ventilation. This dual function of trunk muscles in locomotion and ventilation leads to a biomechanical conflict in many lizards and constrains their ability to breathe while running ("axial constraint") which likely is reflected by their high anaerobic scope. Furthermore, different foraging and predator-escape strategies were shown to correlate with the metabolic profile of locomotor muscles in lizards. Because knowledge of muscle's fiber-type composition may help to reveal a muscle's functional properties, we investigated the distribution pattern of muscle fiber types in the perivertebral musculature in two small lizard species with a generalized body shape and subjected to the axial constraint (Dipsosaurus dorsalis, Acanthodactylus maculatus) and one species that circumvents the axial constraint by means of gular pumping (Varanus exanthematicus). Additionally, these species differ in their predator-escape and foraging behaviors. Using refined enzyme-histochemical protocols, muscle fiber types were differentiated in serial cross-sections through the trunk, maintaining the anatomical relationships between the skeleton and the musculature. The fiber composition in Dipsosaurus and Acanthodactylus showed a highly glycolytic profile, consistent with their intermittent locomotor style and reliance on anaerobic metabolism during activity. Because early representatives of diapsids resemble these two species in several postcranial characters, we suggest that this glycolytic profile represents the plesiomorphic condition for diapsids. In Varanus, we found a high proportion of oxidative fibers in all muscles, which is in accordance with its high aerobic scope and capability of sustained locomotion.

Redescription and phylogenetic relationships of <i>Solenodonsaurus janenschi</i> Broili, 1924, from the Late Carboniferous of Nýřany, Czech Republic

The basal tetrapod <i>Solenodonsaurus janenschi</i> Broili, 1924, from Nýřany (Westphalian D, Late Carboniferous), Czech Republic, is redescribed and its phylogenetic position reevaluated. A distinct groove at the base of the maxillary teeth is regarded as an autapomorphic character, which is present in both the large and small specimens. Other characteristic features, which are not unique to <i>S. janenschi</i>, are: an extension of the lacrimal that forms the anteroventral margin of the orbit; a long posterior extension of the jugal; spool-shaped vertebrae, and small, wedge-like intercentra. A phylogenetic analysis based on the data matrix of Ruta, Coates and Quicke suggests that <i>S. janenschi</i> is the sister taxon of the Lepospondyli. Shared characters include the shape of the vertebrae, non-swollen neural arches, and absence of an intertemporal. Although nested within the amniote stem, <i>S. janenschi</i> is not as closely related to basal amniotes as previously suggested. A rather long, slender humerus argues for a predominantly terrestrial mode of life, and the curved, slender ribs, as well as the comparatively small skull, suggest costal ventilation of the lungs similar to that in amniotes, rather than buccal pumping. The morphology of the shallow squamosal embayment in which an ossified dorsal margin is absent, renders the presence of a tympanum unlikely. <br><br> doi:<a href="http://dx.doi.org/10.1002/mmng.201200003" target="_blank">10.1002/mmng.201200003</a>

Redescription and phylogenetic relationships of Solenodonsaurus janenschi Broili, 1924, from the Late Carboniferous of Nýřany, Czech Republic

Abstract. The basal tetrapod Solenodonsaurus janenschi Broili, 1924, from Nýřany (Westphalian D, Late Carboniferous), Czech Republic, is redescribed and its phylogenetic position reevaluated. A distinct groove at the base of the maxillary teeth is regarded as an autapomorphic character, which is present in both the large and small specimens. Other characteristic features, which are not unique to S. janenschi, are: an extension of the lacrimal that forms the anteroventral margin of the orbit; a long posterior extension of the jugal; spool-shaped vertebrae, and small, wedge-like intercentra. A phylogenetic analysis based on the data matrix of Ruta, Coates and Quicke suggests that S. janenschi is the sister taxon of the Lepospondyli. Shared characters include the shape of the vertebrae, non-swollen neural arches, and absence of an intertemporal. Although nested within the amniote stem, S. janenschi is not as closely related to basal amniotes as previously suggested. A rather long, slender humerus argues for a predominantly terrestrial mode of life, and the curved, slender ribs, as well as the comparatively small skull, suggest costal ventilation of the lungs similar to that in amniotes, rather than buccal pumping. The morphology of the shallow squamosal embayment in which an ossified dorsal margin is absent, renders the presence of a tympanum unlikely. doi: 10.1002/mmng.201200003

Drinking in Snakes: Resolving a Biomechanical Puzzle

Snakes have long been thought to drink with a two-phase buccal-pump mechanism, but observations that some snakes can drink without sealing the margins of their mouths suggest that buccal pumping may not be the only drinking mechanism used by snakes. Here, we report that some snakes appear to drink using sponge-like qualities of specific regions of the oropharyngeal and esophageal mucosa and sponge-compressing functions of certain muscles and bones of the head. The resulting mechanism allows them to transport water upward against the effects of gravity using movements much slower than those of many other vertebrates. To arrive at this model, drinking was examined in three snake species using synchronized ciné and electromyographic recordings of muscle activity and in a fourth species using synchronized video and pressure recordings. Functional data were correlated with a variety of anatomical features to test specific predictions of the buccal-pump model. The anatomical data suggest explanations for the lack of conformity between a buccal-pump model of drinking and the performance of the drinking apparatus in many species. Electromyographic data show that many muscles with major functions in feeding play minor roles in drinking and, conversely, some muscles with minor roles in feeding play major roles in drinking. Mouth sealing by either the tongue or mental scale, previously considered critical to drinking in snakes, is incidental to drinking performance in some species. The sponge mechanism of drinking may represent a macrostomatan exaptation of mucosal folds, the evolution of which was driven primarily by the demands of feeding.

Microvascularization of the interhyoid muscle in larval Xenopus laevis (Daudin): Scanning electron microscopy of vascular corrosion casts and correlative light microscopy

The interhyoid muscle in tadpoles of Xenopus laevis (Daudin) is an important part of the buccal pump, a functional unit that provides unidirectional flow of water through mouth and pharynx. In anuran tadpoles, this flow is crucial in both respiration (gas exchange) and food intake (ingestion). The microvascular anatomy of the interhyoid muscles of 43 tadpoles of X. laevis from developmental stages 49-60 was examined by scanning electron microscopy of vascular corrosion casts and correlative light microscopy of paraplast embedded Goldner stained serial tissue sections. Analysis of vascular corrosion casts of the interhyoid muscle showed that several descending branches of external carotid arteries supplied the interhyoid muscle. Arteries splitted into many arterioles at the dorsal surface of the interhyoid muscle and formed sheaths of longitudinally orientated capillaries around muscle fibers. Postcapillary vessels formed perpendicularly orientated arrays of collecting venules (mean diameter: 15.6 μm), which drained the interhyoid muscle from the ventral surface into external jugular veins. Cast analyses revealed sprouting angiogenesis at the capillary level and nonsprouting angiogenesis at distal domains of the venous system. Both means of angiogenesis that persisted throughout the developmental periods examined are thought to represent a superposition of concurrent developmental and physiological processes. The dense microvascular bed of the interhyoid muscle reflects its high demand for supply with oxygen and nutrients.

Buccal pumping mechanics ofXenopus laevistadpoles: effects of biotic and abiotic factors

Biotic factors such as body size and shape have long been known to influence kinematics in vertebrates. Movement in aquatic organisms can also be strongly affected by abiotic factors such as the viscosity of the medium. We examined the effects of both biotic factors and abiotic factors on buccal pumping kinematics in Xenopus tadpoles using high-speed imaging of an ontogenetic series of tadpoles combined with experimental manipulation of the medium over a 10-fold range of viscosity. We found influences of both biotic and abiotic factors on tadpole movements; absolute velocities and excursions of the jaws and hyoid were greater in higher viscosity fluid but durations of movements were unaffected. Smaller tadpoles have relatively wider heads and more robust hyoid muscles used in buccal expansion and compression. Lever arm ratios were found to be constant at all sizes; therefore, smaller tadpoles have relatively higher resolved muscle forces and, like tadpoles in more viscous medium, displayed higher absolute velocities of jaw and hyoid movements. Nonetheless, small tadpoles drew in water at lower Reynolds numbers (Re) than predicted by kinematics, due to negative allometry of the buccal pump. Finally, tadpoles transitioned from a flow regime dominated by viscous forces (Re=2) to an intermediate regime (Re=106).

The Physical Movement of Urine from the Kidneys to the Urinary Bladder and Bladder Compliance in Two Anurans

Urine movement from the ureters to the bladder was accomplished by a combination of gravity and pressures resulting from lung inflation, buccal pumping, and smooth-muscle contraction. Urine movement from the cloaca to the urinary bladder was the result of pressure generated by cloacal smooth-muscle contraction and opposed by urinary bladder pressure, resulting from compliance, lung inflation, and buccal movements. The frequency of cloacal smooth-muscle contraction measured in Chaunus marinus (4.9 min(-1)) and Lithobates grylio (2.8 min(-1)) generated cloacal pressures that averaged 0.67 and 0.59 kPa, respectively. Chaunus marinus had a mean internal bladder pressure of 0.29 kPa, while Lithobates catesbeiana had a mean internal bladder pressure of 0.16 kPa. Using direct urinary bladder infusion and physiological pressure transducers on live anurans, it was determined that urinary bladder compliance was lower (P < 0.05) in the aquatic frog L. grylio (2,050 mL kPa(-1) kg(-1)) than in the terrestrial toad C. marinus (4,440 mL kPa(-1) kg(-1)). Taken together, these data suggest that bladder filling is a result of pressures generated in the ureters and the cloaca that are greater than internal bladder pressures and that the more aquatic species had a less compliant urinary bladder compared with that of the terrestrial species.

Discrimination of chemical stimuli in conspecific fecal pellets by a visually adept iguanid lizard, Crotaphytus collaris

Iguanid lizards are known for visual acuity and a diminished vomeronasal organ, which has led to mixed conclusions on whether iguanids use chemical cues. The collared lizard, Crotaphytus collaris, is a territorial iguanid that lives in open rocky habitats. Fecal pellets placed prominently on open rocky perches may provide an ideal mechanism for intraspecific chemical signaling. In order to determine whether collared lizards can discriminate between chemical stimuli found in conspecific fecal pellets, we collected 24 males and 25 females to analyze sex-specific behavioral responses via tongue-flicks and a newly observed behavior for the species, gular pumps, to cotton swabs containing water, cologne, chemical stimuli from conspecific male and female fecal pellets, and the lizard’s own fecal pellet. Both sexes were able to discriminate chemical stimuli from water via at least one behavior. Male collared lizards exhibited greater rates of response (tongue-flick and gular pumps) toward male fecal pellets when compared to the negative water control. Our results also suggest individuals may be able to discriminate between fecal pellets, as indicated by generally greater (but non-significant) counts of male tongue-flick responses to male fecal pellets when compared to their own. Collared lizard chemical discrimination appears to utilize tongue-flick and gular pump behaviors, possibly associated with distinct chemosensory modes (vomerolfaction and olfaction). Based on this study, we suggest that chemical signals may play a greater role in intraspecific communication than previously thought in this highly visual lizard.

Measuring the state of consciousness in a free-living diving sea turtle

We report on results from two types of data-logger attached to hawksbill turtles ( Eretmochelys coriacea) in the breeding season at the Seychelles, Indian Ocean. Conventional time–depth recorders (TDRs) showed prolonged bouts of long dives to the seabed, consistent with benthic resting. This behaviour has been widely reported in sea turtles and appears to be a common feature for energy conservation. An Inter-Mandibular Angle Sensor (IMASEN) recorded mouth opening and buccal pumping by one turtle for 2.5 days. Buccal pumping occurred widely while the turtle was submerged, consistent with a function of olfactory sensory perception of the turtle's environment. However, buccal pumping stopped during the middle of long benthic dives consistent with the turtle entering a phase of sleep. It therefore appears that by recording buccal oscillations, it is possible to assess the state of consciousness of turtles allowing the eco-physiology of diving to be more fully explored.

Going to extremes of lung volume

volume changes in the lung are the basis for life-sustaining respiration, yet in many regards, the lung is overengineered and the mechanical limits are most often not approached ([11][1]). For some activities, however, the entire volume range of the thorax and lung is necessary; for example,

Functional morphology and evolution of aspiration breathing in tetrapods

In the evolution of aspiration breathing, the responsibility for lung ventilation gradually shifted from the hyobranchial to the axial musculoskeletal system, with axial muscles taking over exhalation first, at the base of Tetrapoda, and then inhalation as well at the base of Amniota. This shift from hyobranchial to axial breathing freed the tongue and head to adapt to more diverse feeding styles, but generated a mechanical conflict between costal ventilation and high-speed locomotion. Some "lizards" (non-serpentine squamates) have been shown to circumvent this speed-dependent axial constraint with accessory gular pumping during locomotion, and here we present a new survey of gular pumping behavior in the tuatara and 40 lizard species. We observed gular pumping behavior in 32 of the 40 lizards and in the tuatara, indicating that the ability to inflate the lungs by gular pumping is a shared-derived character for Lepidosauria. Gular pump breathing in lepidosaurs may be homologous with buccal pumping in amphibians, but non-ventilatory buccal oscillation and gular flutter have persisted throughout amniote evolution and gular pumping may have evolved independently by modification of buccal oscillation. In addition to gular pumping in some lizards, three other innovations have evolved repeatedly in the major amniote clades to circumvent the speed-dependent axial constraint: accessory inspiratory muscles (mammals, crocodylians and turtles), changing locomotor posture (mammals and birds) and respiratory-locomotor phase coupling to reduce the mechanical conflict between aspiration breathing and locomotion (mammals and birds).

The Vocal Sac Increases Call Rate in the Túngara FrogPhysalaemus pustulosus

In most anurans, the production of advertisement calls is accompanied by the inflation of a vocal sac. Current functions of the vocal sac, however, are not fully understood, although several hypotheses have been proposed. One hypothesis suggests that the vocal sac decreases the intercall interval (i.e., increases call rate) by reinflating the lungs more rapidly than is possible with the buccal pump. We investigate this hypothesis by analyzing audio and video recordings of calling tungara frogs. We compare the first two call bouts emitted by an originally uninflated male. The first call bout requires lung inflation via buccal pumping, but in the second, the male is already inflated because of capture of air and reinflation of the lungs by the vocal sac. Lung inflation to typical field levels requires 26-51 buccal pumps, which takes at least 4.4 s. This estimate is more than 2.5 times the typical intercall interval with lung reinflation via a vocal sac (ca. 1.7 s). Evidence from phonotaxis tests demonstrates that these differences in intercall intervals are salient to females and that female Physalaemus pustulosus prefer the shorter intercall interval/higher call rate. Acoustic analyses demonstrate that the first call of bout 1, which requires buccal pumping, is usually shorter, of lower amplitude, and spans a smaller frequency range than the first call of bout 2, which does not require buccal pumping. Because females prefer longer, more intense calls, these results suggest that the vocal sac not only increases call rate but also allows males to produce more calls of increased attractiveness to females.

Neuroanatomy of the sucking pump of the moth, Manduca sexta (Sphingidae, Lepidoptera)

Knowledge of the neuroanatomy of the sucking pump of Manduca sexta (Sphingidae) is valuable for studies of olfactory learning, pattern generators, and postembryonic modification of motor circuitry. The pump comprises a cibarial valve, a buccal pump, and an esophageal sphincter valve. Cibarial opener and closer muscles control the cibarial valve. Six pairs of dilator muscles and a compressor muscle operate the buccal pump. The cibarial opener and one pair of buccal dilator muscles are innervated by paired neurons in the tritocerebrum, and the cibarial opener has double, bilateral innervation. Their tritocerebral innervation indicates that these muscles evolved from labro-clypeal muscles. The remaining paired buccal dilator muscles each are innervated by an unpaired motor neuron in the frontal ganglion. These motor neurons project bilaterally through the frontal connectives to dendritic arborizations in the tritocerebrum. These projections also have a series of dendritic-like arborizations in the connectives. The cibarial closer and buccal compressor muscles are also innervated by motor neurons in the frontal ganglion, but only the closer muscle neuron projects bilaterally to the tritocerebrum. The innervation of the pump muscles indicates that they are associated with the stomodaeum, and, therefore, the buccal pump evolved from the anterior stomodaeum rather than from the cibarium.

Elevated intra-abdominal pressure limits venous return during exercise inVaranus exanthematicus

The effects of treadmill exercise on components of the cardiovascular (venous return, heart rate, arterial blood pressure) and respiratory systems (minute ventilation, tidal volume, breathing frequency, oxygen consumption, carbon dioxide production) and intra-abdominal pressure were investigated in the Savannah monitor lizard, Varanus exanthematicus B., at 35 degrees C. Compared with resting conditions, treadmill exercise significantly increased lung ventilation, gular pumping, intra-abdominal pressure, mean arterial blood pressure and venous return (blood flow in the post caval vein). However, venous return declines at high levels of activity, and mean arterial pressure and venous return did not attain peak values until the recovery period, immediately following activity. Elevating intra-abdominal pressure in resting lizards (via saline infusion) resulted in significant reductions in venous return when the transmural pressure of the post caval vein became negative (i.e. when intra-abdominal pressure exceeded central venous pressure). Together these results suggest that increments in intra-abdominal pressure compress the large abdominal veins and inhibit venous return. During locomotion, the physical compression of the large abdominal veins may represent a significant limitation to cardiac output and maximal oxygen consumption in lizards.

Vertebrate lungs: structure, topography and mechanics

Vertebrate lungs are highly diverse in their structure, topographical position, ventilation mechanisms, constructional integration into the locomotor apparatus, and the interrelationships with the mode of their ontogenetic development. Vertebrate lungs evolved as supplementary air-breathing organs in primary fishes, being ventilated by buccal pumping. In most recent fishes the lungs are transformed into the hydrostatic swimbladder. This basic type of unicameral lungs and their buccal pumping ventilation are also found in recent amphibians. Land vertebrates developed a very efficient aspiration type of ventilation. In most recent reptiles the lungs are subdivided into three rows of lung chambers, enlarging the exchange surface in correlation to their increasing metabolic needs. The avian respiratory apparatus, with its volume-constant lungs and highly compliant air sacs, and the mammalian broncho-alveolar lung, with its very low compliance, are both derived from multicameral lungs. The avian and the mammalian respiratory systems are integrated very differently with the specific constructions of their locomotor apparatusses and the specific mode of their ontogenetic development.

Avenues of extrapulmonary oxygen uptake in western painted turtles ( Chrysemys picta belli) at 10 °C

The major avenues of extrapulmonary oxygen uptake were determined on submerged western painted turtles ( Chrysemys picta bellii) at 10 °C by selectively blocking one or more potential pathways for exchange. Previous work indicated that the skin, the cloaca, and the buccopharyngeal cavity can all contribute significantly in various species of turtles. O 2 uptake was calculated from the rate of fall in water P O 2 in a closed chamber. Two series of experiments were conducted: in Series 1, each of the potential avenues was mechanically blocked either singly or in combination; in Series 2, active cloacal and buccal pumping were prevented pharmacologically using the paralytic agent rocuronium. In addition in Series 2, N 2-breathing preceded submergence in some animals and in one set of Series 2 experiments arterial blood was sampled and analyzed for pH, lactate, P O 2 , and P CO 2 . Results in both Series 1 and Series 2 revealed that prevention of cloacal and/or buccopharyngeal exchange did not significantly affect total O 2 uptake. Interfering with skin diffusion in Series 1, however, significantly reduced O 2 uptake by 50%. N 2-breathing prior to submergence in Series 2 did not affect O 2 uptake in paralyzed turtles but significantly increased uptake in unparalyzed turtles without catheters. Blood analysis revealed that all submerged turtles developed lactic acidosis, but the rate of rise in lactate was significantly lower in paralyzed animals. We conclude that passive diffusion through the integument is the principal avenue of aquatic O 2 uptake in this species.

Ventilatory behaviors of the toad Bufo marinus revealed by coherence analysis.

Breathing in amphibians is a remarkably complex behavior consisting of irregular breaths that may be taken singly or in bouts that are used to deflate and inflate the lungs. The valves at the two outlets of the buccal cavity (nares and glottis) need to be finely controlled throughout the bout for the expression of these complex respiratory behaviors. In this study, we use a technique based on the calculation of the coherence spectra between respiratory variables (buccal pressure; narial airflow; and lung pressure). Coherence was also used to quantify the effects of chemoreceptor and pulmonary mechanoreceptor input on narial and glottal valve behavior on normoxic, hypoxic, and hypercapnic toads with both intact and bilaterally sectioned pulmonary vagi. We found a significant reduction in narial coherence in hypoxic vagotomized toads indicating that pulmonary mechanoreceptor feedback modulates narial opening duration. An unexpectedly high coherence between Pl and Pb during non-respiratory buccal oscillations in hypercapnic toads indicated more forceful use of the buccal pump. We concluded that the coherence function reveals behaviors that are not apparent through visual inspection of ventilatory time series.