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Functional morphology and evolution of aspiration breathing in tetrapods
Abstract
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).
... We used the character-taxon matrix from Clack et al. [37] as a basis for the updated and expanded matrix used in this study. The subsequent compound characters from Clack et al. [37] were split following Brazeau [63]: 7,22,62,82,103,111,112,113,123,135,136,146,156,160,180,195,196,210,236,238,240,284,285. Three new characters were added or modified from Kissel [40]. ...
... These authors suggested that a shift in the primary mode of respiration from buccal pumping in non-amniote tetrapods to costal respiration in amniotes relieved a constraint on skull anatomy and allowed for its diversification into forms suitable for herbivory. Buccal pumping is the ancestral mode of respiration for tetrapods [108][109][110][111], involving expansion and contraction of the buccal cavity to pump air into the lungs under positive pressure. Costal respiration, on the other hand, involves the expansion and contraction of the rib cage to fill the lungs. ...
... Non-amniote tetrapods plesiomorphically possess short, immobile ribs that are incapable of this movement [107]. All extant amniotes are capable of costal respiration [108,109], yet an advanced form of buccal pumping alongside costal respiration is retained in some lepidosaurs [111,112]. Thus, costal respiration likely evolved as an alternative to buccal pumping along the lineage leading to Amniota and functions as the primary mode of respiration in most taxa. ...
Among terrestrial tetrapods, the origin of herbivory marked a key evolutionary event that allowed for the evolution of modern terrestrial ecosystems. A 100 Ma gap separates the oldest terrestrial tetrapods and the first undisputed herbivorous tetrapods. While four clades of early tetrapod herbivores are undisputed amniotes, the phylogenetic position of Diadectomorpha with respect to Amniota has long been controversial. Given that the origin of herbivory coincides with the oldest amniotes, and obligate herbivory is unknown within amphibians, this suggests that a key adaptation necessary to evolve obligate herbivory is unique to amniotes. Historically, phylogenetic analyses have found Diadectomorpha as the sister-group to amniotes, but recent analyses recover Diadectomorpha as sister-group to Synapsida, within Amniota. We tested whether diadectomorphs are amniotes by updating the most recent character–taxon matrix. Specifically, we added new characters from the lower jaw and added diadectomorph taxa, resulting in a dataset of 341 characters and 61 operational taxonomic units. We updated the description of five diadectomorph jaws using microcomputed tomography data. Our majority-rule consensus places Diadectomorpha as sister-group to Synapsida; other methods do not recover this relationship. We revise diadectomorph taxonomy, erecting a new species from the early Permian Bromacker locality, Germany, and a new genus to accommodate ‘Diadectes’ sanmiguelensis.
... In air breathing vertebrates (e.g., amphibians), comingling of the lungs and digestive tract was fine when breathing was accomplished by buccal or positive pressure breathing (Fig. 4). However, in reptiles, aspiration breathing evolved to facilitate the external circulation of air into the lungs for gas exchange (69,503). The strategy of aspiration breathing in reptiles was critical for more efficient external circulation of air into the lungs. ...
... The earliest strategy for distributing fresh air into the lungs was buccal breathing (Fig. 4) (64,66,69,399,414,415). In this scenario, the oral cavity expands and compresses, with air forced into the lung under positive pressure. ...
... In rayfinned fishes, buccal breathing serves to perfuse the gill with water. In lungfish and the extant amphibians, it serves to inflate the lung (64,66,69,399,414,415). At some point in the early natural history of the amniotes (reptiles, mammals, and birds), aspiration breathing evolved, a strategy whereby the lungs are inflated by the generation of a subatmospheric negative pressure to cause influx of atmospheric air (64,66,69,399,414,415,503). ...
Symmorphosis is a concept of economy of biological design, whereby structural properties are matched to functional demands. According to symmorphosis, biological structures are never over designed to exceed functional demands. Based on this concept, the evolution of the diaphragm muscle (DIAm) in mammals is a tale of two structures, a membrane that separates and partitions the primitive coelomic cavity into separate abdominal and thoracic cavities and a muscle that serves as a pump to generate intra‐abdominal (Pab) and intrathoracic (Pth) pressures. The DIAm partition evolved in reptiles from folds of the pleural and peritoneal membranes that was driven by the biological advantage of separating organs in the larger coelomic cavity into separate thoracic and abdominal cavities, especially with the evolution of aspiration breathing. The DIAm pump evolved from the advantage afforded by more effective generation of both a negative Pth for ventilation of the lungs and a positive Pab for venous return of blood to the heart and expulsive behaviors such as airway clearance, defecation, micturition, and child birth. © 2019 American Physiological Society. Compr Physiol 9:715‐766, 2019.
... Costal aspiration, in which motions of the ribs are used to ventilate the lungs, is the ancestral mode of ventilation for amniotes (Janis and Keller 2001;Brainerd and Owerkowicz 2006). Rib motions continue to contribute to ventilation mechanisms in all extant amniotes except turtles, and although apparently simple, these movements are deceptively complex. ...
... In contrast, I. iguana are predominantly sedentary, foraging in trees and relying on crypsis and only brief bouts of activity to avoid predation (Greene et al. 1978). While the axial conflict between ventilation and locomotion is ancestral for Amniota, numerous muscular and skeletal innovations have evolved to reduce the negative effects of locomotion on ventilation, including modifications of costovertebral morphology (Brainerd and Owerkowicz 2006;Claessens 2015). ...
... Many squamates use rib rotations to affect large body shape changes for behaviors such as defensive inflation, defensive or offensive displays such as the hooding of cobras, escaping into narrow crevices, crypsis, flattening for basking, and even gliding through the air (Deban et al. 1994;Stuart-Fox et al. 2006;Young and Kardong 2010;McGuire and Dudley 2011;Socha 2011;Lillywhite 2014;Cieri 2018). Squamates are also the only extant amniote group to remain susceptible to the ancestral axial conflict between locomotion and ventilation and therefore lack substantial locomotor stamina (Brainerd and Owerkowicz 2006). Without the ability to flee for extended periods of time, the ability to fit into extremely tight spaces or deter predators through postural displays and body shape changes would have been beneficial. ...
Rib rotations contribute to lung ventilation in most extant amniotes. These rotations are typically described as bucket-handle rotation about a dorsoventral axis, caliper rotation about a craniocaudal axis, and pump-handle rotation about a mediolateral axis. A synapomorphy for Lepidosauria is single-headed costovertebral articulations derived from the ancestral double-headed articulations of most amniotes. With a single articular surface, the costovertebral joints of squamates have the potential to rotate with three degrees-of-freedom (DOFs), but considerable variation exists in joint shape. We compared the costovertebral morphology of the Argentine black and white tegu, Salvator merianae, with the green iguana, Iguana iguana, and found that the costovertebral articulations of I. iguana were hemispherical, while those of S. merianae were dorsoventrally elongated and hemiellipsoidal. We predicted that the elongate joints in S. merianae would permit bucket-handle rotations while restricting caliper and pump-handle rotations, relative to the rounded joints of I. iguana. We used X-ray reconstruction of moving morphology to quantify rib rotations during breathing in S. merianae for comparison with prior work in I. iguana. Consistent with our hypothesis, we found less caliper motion in S. merianae than in I. iguana, but unexpectedly found similar pump-handle magnitudes in each species. The dorsoventrally elongate costovertebral morphology of S. merianae may provide passive rib support to reduce the conflict between locomotion and ventilation. Moreover, the observation of multiple DOFs during rib rotations in both species suggests that permissive costovertebral morphology may be more related to the biological roles of ribs outside of ventilation and help explain the evolution of this trait.
... What is the relationship between the design of the lung and the trunk in vertebrates? The use of costal inspiration and expiration is likely to be the basal condition for amniotes (Brainerd and Owerkowicz, 2006), so it is reasonable to expect that amniote ribs are designed primarily to effect ventilation by moving to generate sub-and super-atmospheric pressures in the thoracic cavity, and that the lung is designed primarily to be ventilated in this manner. Both structures, however, are affected by other parts of the body. ...
... The trunk functions in body support and locomotion, either by providing a stable chassis for motions of the limbs (Carrier, 1990;Carrier, 1993;Ritter, 1995Ritter, , 1996 or by generating locomotor work itself by lateral (Ritter, 1996) or dorsoventral (Carrier, 1996) oscillation. Lungs may also be ventilated by accessory trunk muscles such as diaphragms (Gans and Clark, 1976;Bramble and Jenkins, 1993;Farmer and Carrier, 2000), motion of the appendicular skeleton (Boggs et al., 1997;Boggs, 2002), cardiogenic oscillation (Szecwak and Jackson, 1992;Farmer, 2010) and gular pumping (Brainerd and Owerkowicz, 2006). The interactions between the trunk and lung are therefore far from straightforward. ...
... Squamates are a good group for investigating lung-trunk interactions because they lack accessory breathing mechanisms, such as the diaphragm of mammals or sternal pump of birds (Carrier, 1987;Claessens, 2009), and therefore rely primarily on costal movements for lung ventilation (Brainerd and Owerkowicz, 2006). Costal anatomy varies greatly among squamates, with species showing variable numbers of both true and floating ribs consisting of one to three different segments (Hoffstetter and Gasc, 1969). ...
The structures and functions of the vertebrate lung and trunk are linked through the act of ventilation, but the connections between these structures and functions are poorly understood. We used XROMM to measure rib kinematics during lung ventilation in three savannah monitor lizards, Varanus exanthematicus All of the dorsal ribs, including the floating ribs, contributed to ventilation; the magnitude and kinematic pattern showed no detectable cranial-to-caudal gradient. The true ribs acted as two rigid bodies connected by flexible cartilage, with the vertebral rib and ventromedial shaft of each sternal rib remaining rigid and the cartilage between them forming a flexible intracostal joint. Rib rotations can be decomposed into bucket handle rotation around a dorsoventral axis, pump handle rotation around a mediolateral axis, and caliper motion around a craniocaudal axis. Dorsal rib motion was dominated by roughly equal contributions of bucket and pump rotation in two individuals and by bucket rotation in the third individual. The recruitment of floating ribs during ventilation in monitors is strikingly different from the situation in iguanas, where only the first few true ribs contribute to breathing. This difference may be related to the design of the pulmonary system and life history traits in these two species. Motion of the floating ribs may maximize ventilation of the caudally and ventrolaterally-positioned compliant saccular chambers in the lungs of varanids, while restriction of ventilation to a few true ribs may maximize crypsis in iguanas.
... The mechanics of the hepatic piston are relatively straightforward and have been extensively studied Uriona and Farmer, 2006;Munns et al., 2012), but costal aspiration is more complex. Ventilation is powered by the hypaxial muscles, with the transverse abdominal responsible for exhalation, and the intercostal muscles powering inhalation and exhalation (Gans and Clark, 1976;Carrier, 1989;Brainerd and Owerkowicz, 2006). However, muscles can only do positive work and hence contribute to ventilation when actively shortening, but in order to power inhalation this muscular contraction must be converted into expansion of the thorax (Brainerd and Owerkowicz, 2006;Brainerd, 2015). ...
... Ventilation is powered by the hypaxial muscles, with the transverse abdominal responsible for exhalation, and the intercostal muscles powering inhalation and exhalation (Gans and Clark, 1976;Carrier, 1989;Brainerd and Owerkowicz, 2006). However, muscles can only do positive work and hence contribute to ventilation when actively shortening, but in order to power inhalation this muscular contraction must be converted into expansion of the thorax (Brainerd and Owerkowicz, 2006;Brainerd, 2015). ...
... Crocodylians, along with almost all other amniotes (turtles are one notable exception; Lyson et al., 2014), possess a mobile ribcage, which forms a musculoskeletal lever system, and it is this lever system that allows the conversion of intercostal muscle shortening into thoracic expansion (Brainerd and Owerkowicz, 2006;Brainerd, 2015). Given their essential role in costal aspiration, it is important to understand the form-function relationship between ribcage morphology and the mechanics of thoracic volume change, particularly in crocodylians, as they serve as our best extant model for fossil archosaurs (Claessens, 2015). ...
The current hypothesis regarding the mechanics of breathing in crocodylians is that the double-headed ribs, with both a capitulum and tuberculum, rotate about a constrained axis passing through the two articulations; moreover, this axis shifts in the caudal thoracic ribs, as the vertebral parapophysis moves from the centrum to the transverse process. Additionally, the ventral ribcage in crocodylians is thought to possess additional degrees of freedom through mobile intermediate ribs. In this study, X-ray reconstruction of moving morphology (XROMM) was used to quantify rib rotation during breathing in American alligators. Whilst costovertebral joint anatomy predicted overall patterns of motion across the ribcage (decreased bucket handle motion and increased calliper motion), there were significant deviations: anatomical axes overestimated pump handle motion and, generally, ribs in vivo rotate about all three body axes more equally than predicted. The intermediate ribs are mobile, with a high degree of rotation measured about the dorsal intracostal joints, especially in the more caudal ribs. Motion of the sternal ribs became increasingly complex caudally, owing to a combination of the movements of the vertebral and intermediate segments. As the crocodylian ribcage is sometimes used as a model for the ancestral archosaur, these results have important implications for how rib motion is reconstructed in fossil taxa, and illustrate the difficulties in reconstructing rib movement based on osteology alone.
... Extant amphibians and lung-breathing fishes fill their lungs by vertical movements of the buccal floor that press air from the buccal cavity into the lungs without involvement of trunk musculature (buccal pump mechanism; Brainerd, 1999). In contrast, extant amphibians (but not fishes) use contraction of the transverse abdominal musculature for exhalation (Brainerd et al., 1993;Brainerd, 1998;Brainerd and Monroy, 1998;Brainerd and Simons, 2000;Simons et al., 2000;Brainerd and Owerkowicz, 2006). The straight, short ribs of extant amphibians play no functional role in lung breathing. ...
... The straight, short ribs of extant amphibians play no functional role in lung breathing. In contrast, the lungs of amniotes are ventilated by movements of the rib cage (aspiration pump): action of the trunk muscles expands the thorax, generates negative pressure in the lungs, and air is drawn in (Brainerd, 1999;Brainerd and Owerkowicz, 2006;Brainerd et al., 2016). ...
... The extant phylogenetic bracket suggests that Archegosaurus used its ventral trunk musculature, the m. transversus abdominis, for forcing air out of the lungs because this muscle is employed in exhalation in both amniotes and extant amphibians (Brainerd et al., 1993;Brainerd and Owerkowicz, 2006). ...
Physiological aspects like heat balance, gas exchange, osmoregulation, and digestion of the early Permian aquatic temnospondyl Archegosaurus decheni, which lived in a tropical freshwater lake, are assessed based on osteological correlates of physiologically relevant soft-tissue organs and by physiological estimations analogous to air-breathing fishes. Body mass (M) of an adult Archegosaurus with an overall body length of more than 1 m is estimated as 7 kg using graphic double integration. Standard metabolic rate (SMR) at 20 °C (12 kJ h⁻¹) and active metabolic rate (AMR) at 25 °C (47 kJ h⁻¹) were estimated according to the interspecific allometry of metabolic rate (measured as oxygen consumption) of all fish (VO2 = 4. 8 M0. 88) and form the basis for most of the subsequent estimations. Archegosaurus is interpreted as a facultative air breather that got O2 from the internal gills at rest in well-aerated water but relied on its lungs for O2 uptake in times of activity and hypoxia. The bulk of CO2 was always eliminated via the gills. Our estimations suggest that if Archegosaurus did not have gills and released 100 % CO2 from its lungs, it would have to breathe much more frequently to release enough CO2 relative to the lung ventilation required for just O2 uptake. Estimations of absorption and assimilation in the digestive tract of Archegosaurus suggest that an adult had to eat about six middle-sized specimens of the acanthodian fish Acanthodes (ca. 8 cm body length) per day to meet its energy demands. Archegosaurus is regarded as an ammonotelic animal that excreted ammonia (NH3) directly to the water through the gills and the skin, and these diffusional routes dominated nitrogen excretion by the kidneys as urine. Osmotic influx of water through the gills had to be compensated for by production of dilute, hypoosmotic urine by the kidneys. Whereas Archegosaurus has long been regarded as a salamander-like animal, there is evidence that its physiology was more fish- than tetrapod-like in many respects.
... Extant amphibians (and lung-breathing fishes) inhale air via a buccal pump mechanism ('air gulping'), that is vertical movements of the buccal floor press air from the buccal cavity into the lungs without involvement of trunk musculature (Gans 1970a,b;Brainerd 1999). In contrast, exhalation is driven by contraction of the transverse musculature in extant amphibians (Brainerd et al. 1993;Brainerd & Owerkowicz 2006). The straight, short ribs of amphibians are not involved in breathing, and they have often proportionally large, broad and flattened skulls, so that a large volume of air can be pressed into the lungs with a single 'gulp' (Szarski 1962;Schmalhausen 1968). ...
... The straight, short ribs of amphibians are not involved in breathing, and they have often proportionally large, broad and flattened skulls, so that a large volume of air can be pressed into the lungs with a single 'gulp' (Szarski 1962;Schmalhausen 1968). In amniotes, lungs are ventilated by the aspiration pump, that is movements of the rib cage: expansion of the thorax by trunk musculature generates negative pressure and air is subsequently drawn into the lungs (Brainerd 1999; Brainerd & Owerkowicz 2006). Costal aspiration is the much more efficient mode of lung ventilation because it permits faster rates of ventilation and gas exchange (Janis & Keller 2001). ...
... Because aspiration breathing allowed for the release of a large amount of CO 2 via the lungs, it was possible to reduce internal gills completely already in early stem amniotes. Despite the evolution of the aspiration pump, some stem amniotes might still have used buccal bumping as an accessory mechanism of lung ventilation, as indicated by the presence of a gular pump in extant monitor lizards, which may have been retained from the buccal pump of early tetrapods (Owerkowicz et al. 2001;Brainerd & Owerkowicz 2006). Furthermore, it cannot be ruled out that the small size and elongate shape of many lepospondyls such as 'microsaurs', lysorophians or a€ ıstopods permitted skin respiration to a certain degree (Schoch & Carroll 2003); however, rib morphology strongly suggests that the aspiration pump was the major breathing mechanism (and the lungs the major site of CO 2 -release) also in these forms. ...
One of the most important physiological changes during the conquest of land by vertebrates was the increasing reliance on lung breathing, with the concomitant decrease in importance of gill breathing. The main problem involved here was to cope with the excessive accumulation of CO2 in the body and to avoid respiratory acidosis. In the past, several often mutually contradicting hypotheses of CO2-elimination via skin, lungs and gills in early tetrapods have been proposed, based on theoretical physiological considerations and comparison with extant air-breathing fishes and amphibians. This study proposes a revised scenario of CO2-elimination in early tetrapods based on fossil evidence, that is recently identified osteological correlates of gills, skin structure and mode of lung ventilation. In stem tetrapods of the Devonian and Carboniferous, O2-uptake via the lungs by buccal pumping was decoupled from CO2-release via internal gills, and the rather gas-impermeable skin played a minor role in gaseous exchange. The two main lineages of crown-group tetrapods, the amphibian and amniote lineage, used different strategies of CO2-elimination. As in stem tetrapods, O2-uptake and CO2-release remained always largely decoupled in temnospondyls, which ventilated their lungs via buccal pumping and relied mainly on their internal gills for CO2-release. Temnospondyls were not able to reduce their internal gills before their skin became more gas permeable and their body size was reduced, to shift from internal gills to the skin as the major site of CO2-elimination, a pattern that is retained in most lissamphibians. In contrast, internal gills were lost very early in stem amniote evolution. This was associated with the evolution of the more effective aspiration pump that allowed the elimination of the bulk of CO2 via the lungs, leading to a coupled O2-uptake and CO2-loss in stem amniotes and later in amniotes.
... Passive exhalation is still the norm in the other two major groups of amphibians [Anurans (frogs) and Gymnophionans (caecilians)] but both these groups have highly specialized body shapes and modes of locomotion raising the possibility that active expiration was an ancestral trait that was secondarily lost in both groups (118). If so, this suggests that the ability to recruit axial muscles innervated by spinal motoneurons, for exhalation is a shared-derived character found in all tetrapods. ...
... The second step in the evolution of aspiration breathing was to use axial muscles for both inspiration and expiration (118) (Figure 3). While the need for a buccal pump became reduced, remnants of this behavior can still be recruited in all tetrapods (13,15,113,220,857,1223). ...
The ectothermic vertebrates are a diverse group that includes the Fishes (Agnatha, Chondrichthyes, and Osteichthyes), and the stem Tetrapods (Amphibians and Reptiles). From an evolutionary perspective, it is within this group that we see the origin of air-breathing and the transition from the use of water to air as a respiratory medium. This is accompanied by a switch from gills to lungs as the major respiratory organ and from oxygen to carbon dioxide as the primary respiratory stimulant. This transition first required the evolution of bimodal breathing (gas exchange with both water and air), the differential regulation of O2 and CO2 at multiple sites, periodic or intermittent ventilation, and unsteady states with wide oscillations in arterial blood gases. It also required changes in respiratory pump muscles (from buccopharyngeal muscles innervated by cranial nerves to axial muscles innervated by spinal nerves). The question of the extent to which common mechanisms of respiratory control accompany this progression is an intriguing one. While the ventilatory control systems seen in all extant vertebrates have been derived from common ancestors, the trends seen in respiratory control in the living members of each vertebrate class reflect both shared-derived features (ancestral traits) as well as unique specializations. In this overview article, we provide a comprehensive survey of the diversity that is seen in the afferent inputs (chemo and mechanoreceptor), the central respiratory rhythm generators, and the efferent outputs (drive to the respiratory pumps and valves) in this group. © 2022 American Physiological Society. Compr Physiol 12: 1-120, 2022.
... As adults, even though the gills have regressed, they continue to ventilate the buccal cavity in a manner believed to be homologous with gill ventilation. Furthermore, the amphibians are the first group to exhibit active expiration involving thoraco-abdominal muscles (Brainerd and Owerkowicz, 2006). The evolution of active inspiration (aspiration via suction) appears only in the amniotes (Fig. 2). ...
... Furthermore, developmental disruption of rhombomere 4 results in lethal mutations attributed to respiratory failure (Borday et al., 2004;Champagnat et al., 2009;Chatonnet et al., 2003). An axial muscle-based expiration (the expiration pump) is also found in urodele amphibians (salamanders) and is believed to have arisen in the common ancestor of all tetrapods (Brainerd, 1994(Brainerd, , 1998Brainerd and Owerkowicz, 2006) (Fig. 2). As noted earlier, while active expiration is not present in most anuran amphibians under resting conditions, it is present in Xenopus even during routine lung ventilation (de Jongh, 1972) and in all frogs during vocalization (Brainerd, 1999;Marsh and Taigen, 1987;Martin and Gans, 1972). ...
Tracing the evolution of the central rhythm generators associated with ventilation in vertebrates is hindered by a lack of information surrounding key transitions. To begin with, central rhythm generation has been studied in detail in only a few species from four vertebrate groups, lamprey, anuran amphibians, turtles, and mammals (primarily rodents). Secondly, there is a lack of information regarding the transition from water breathing fish to air breathing amniotes (reptiles, birds, and mammals). Specifically, the respiratory rhythm generators of fish appear to be single oscillators capable of generating both phases of the respiratory cycle (expansion and compression) and projecting to motoneurons in cranial nerves innervating bucco-pharyngeal muscles. In the amniotes we find oscillators capable of independently generating separate phases of the respiratory cycle (expiration and inspiration) and projecting to pre-motoneurons in the ventrolateral medulla that in turn project to spinal motoneurons innervating thoracic and abdominal muscles (reptiles, birds, and mammals). Studies of the one group of amphibians that lie at this transition (the anurans), raise intriguing possibilities but, for a variety of reasons that we explore, also raise unanswered questions. In this review we summarize what is known about the rhythm generating circuits associated with breathing that arise from the different rhombomeric segments in each of the different vertebrate classes. Assuming oscillating circuits form in every pair of rhombomeres in every vertebrate during development, we trace what appears to be the evolutionary fate of each and highlight the questions that remain to be answered to properly understand the evolutionary transitions in vertebrate central respiratory rhythm generation.
... Vertebrate trunk muscles can have multifaceted functions in locomotion, body support and respiration (Carrier, 1987;Codd et al., 2005;Farmer & Carrier, 2000a;O'Reilly et al., 2000;Schilling, 2011). Understanding the inter-and intra-specific variations in the functional anatomy of the trunk can reveal adaptations that facilitate simultaneous breathing and locomotion (Brainerd & Owerkowicz, 2006;Carrier, 1991;Lambertz & Perry, 2015). Crocodilians are an interesting group in which to examine these adaptations as they have diverse breathing mechanics and locomotor modes (Codd et al., 2005;Codd et al., 2019;Farmer & Carrier, 2000a;Gans & Clark, 1976). ...
... With the evolution of the respiratory roles of these pumps came a biomechanical constraint on simultaneous breathing and locomotion for early amniotes, Carrier's constraint (Carrier, 1987(Carrier, , 1991. However, most extant amniote groups have evolved accessory breathing mechanisms to overcome this constraint (Brainerd & Owerkowicz, 2006;. In crocodilians, breathing and locomotion are decoupled by their upright gait, derived accessory breathing muscles and transverse processes on the vertebrae that function as attachment sites for epaxial muscles, thereby reducing lateral trunk bending (Farmer & Carrier, 2000b). ...
Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross‐sectional area [PCSA]) and investigate their scaling in juvenile Alligator mississippiensis spanning an order of magnitude in body mass (359 g–5.5 kg). Comparatively, the expiratory muscles (transversus abdominis, rectus abdominis, iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force‐generating capacity, while the inspiratory muscles (diaphragmaticus, truncocaudalis ischiotruncus, ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessory diaphragmaticus scaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. The iliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force‐generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of the diaphragmaticus and compliance of the body wall in the lumbar region against which it works may contribute to low‐cost breathing in crocodilians. The figure shows the head and upper torso of an American alligator.
... Although the exact role of the ribs during snake locomotion remains elusive, it is abundantly clear that snakes use their ribs for a wide array of behaviors. Rib rotations contribute to cross-sectional body shape changes that help generate lift and enable gliding between trees (Socha 2011), mediolateral compression to increase swimming performance (Pattishall and Cundall 2008), production of an edge to dig into the sand for crypsis (Young and Morain 2003), dorsoventrally flattening to increase surface area during basking (Greene 1997), threatening body inflation during hissing (Lillywhite 2014), defensive signaling during hooding (Greene 1997;Young and Kardong 2010;Lillywhite 2014), and the volume changes associated with an ancestral function of ribs for all amniotes, lung ventilation (Rosenberg 1973;Brainerd and Owerkowicz 2006). Moreover, as squamates, snakes' ribs are highly mobile and have the capacity to rotate about three potential axes of rotation, colloquially described as (1) "bucket handle" rotation about a dorsoventral axis ( Fig (Jordanoglou 1970;Osmond 1985). ...
... This alignment has been hypothesized to function as a skeletal strut that dissipates locomotor forces away from the rib cage. In the absence of this morphology, axial musculature typically used for ventilation is co-opted to stabilize limbed locomotor reaction forces, constraining ventilation during locomotion (Carrier 1990(Carrier , 1991Brainerd and Owerkowicz 2006). This negative influence of locomotion on ventilation is thought to be reduced by strut-like costovertebral joints, transferring energy into the axial skeleton rather than requiring muscular stabilization (Claessens 2015;Capano et al. 2019aCapano et al. , 2019b. ...
Locomotion in most tetrapods involves coordinated efforts between appendicular and axial musculoskeletal systems, where interactions between the limbs and the ground generate vertical (GV), horizontal (GH), and mediolateral (GML) ground-reaction forces that are transmitted to the axial system. Snakes have a complete absence of external limbs and represent a fundamental shift from this perspective. The axial musculoskeletal system of snakes is their primary structure to exert, transmit, and resist all motive and reaction forces for propulsion. Their lack of limbs makes them particularly dependent on the mechanical interactions between their bodies and the environment to generate the net GH they need for forward locomotion. As organisms that locomote on their bellies, the forces that enable the various modes of snake locomotion involve two important structures: the integument and the ribs. Snakes use the integument to contact the substrate and produce a friction-reservoir that exceeds their muscle-induced propulsive forces through modulation of scale stiffness and orientation, enabling propulsion through variable environments. XROMM work and previous studies suggest that the serially repeated ribs of snakes change their cross-sectional body shape, deform to environmental irregularities, provide synergistic stabilization for other muscles, and differentially exert and transmit forces to control propulsion. The costovertebral joints of snakes have a biarticular morphology, relative to the unicapitate costovertebral joints of other squamates, that appears derived and not homologous with the ancestral bicapitate ribs of Amniota. Evidence suggests that the biarticular joints of snakes may function to buttress locomotor forces, similar to other amniotes, and provide a passive mechanism for resisting reaction forces during snake locomotion. Future comparisons with other limbless lizard taxa are necessary to tease apart the mechanics and mechanisms that produced the locomotor versatility observed within Serpentes.
... If the ribs were rotating bilaterally to produce lung ventilation in the same stride, then the ventilatory motions would add to the magnitude of one side and subtract from the other. Varanids 28 , but not teiids 29,30 , gular pump during exercise, so we also rejected any locomotor strides in which changes in gular cavity volume were visible in the X-ray movies. Breaths or gular pumps small enough to be unnoticed in the trial selection process would also be too small to significantly affect our kinematic results. ...
... The primitive condition for tetrapods is buccal pump ventilation, where air is forced into the lungs by the musculature of the head. Costal aspiration breathing most likely evolved in stem amniotes 29,31 and represents a shift from the musculoskeletal system of the head being responsible for lung ventilation to the musculoskeletal system of the trunk taking over the responsibility for ventilation. An intermediate step in this transformation is the use of trunk muscles to power expiration while retaining the buccal pump for inspiration, as seen in extant amphibians [32][33][34] . ...
Most lizards walk and run with a sprawling gait in which the limbs are partly advanced by lateral undulation of the axial skeleton. Ribs and vertebrae are integral to this locomotor mode, but 3D motion of the axial skeleton has not been reported for lizard locomotion. Here, we use XROMM to quantify the relative motions of the vertebrae and ribs during slow treadmill locomotion in three savannah monitor lizards (Varanus exanthematicus) and three Argentine black and white tegus (Salvator merianae). To isolate locomotion, we selected strides with no concurrent lung ventilation. Rib rotations can be decomposed into bucket-handle rotation around a dorsoventral axis, pump-handle rotation around a mediolateral axis, and caliper rotations around a craniocaudal axis. During locomotion, every rib measured in both species rotated substantially around its costovertebral joint (8–17 degrees, summed across bucket, pump and caliper rotations). In all individuals from both species, the middle ribs rotated cranially through bucket and pump-handle motion during the propulsive phase of the ipsilateral forelimb. Axial kinematics during swing phase of the ipsilateral forelimb were mirror images of the propulsive phase. Although further work is needed to establish what causes these rib motions, active contraction of the hypaxial musculature may be at least partly responsible. Unilateral locomotor rib movements are remarkably similar to the bilateral pattern used for lung ventilation, suggesting a new hypothesis that rib motion during locomotion may have been an exaptation for the evolution of costal aspiration breathing in stem amniotes.
... In the earliest air-breathing fish and amphibians, the primitive lung's airways smooth muscle contributed significantly to emptying the lung sacs. Air is actively forced into the primitive lungs by muscles in the upper airways while emptying is also an active process driven by largely the smooth muscle of the lower airway (159)(160)(161)(162)(163)(164). Of note, much of the control mechanisms via the vagus nerve appears to have been established at the very earliest stages in the evolution of the lung and air breathing, while surfactants also date back to the earliest lungs and swim bladders (165)(166)(167)(168)(169)(170)(171). ...
... Post-natally, airways caliber is tightly controlled. There is evidence of relatively slow phasic contractions (164,(193)(194)(195)(196)(197)(198)(199)(200)(201)(202)(203)(204), presumably due to ASM length oscillating around an optimal mean. These oscillations appear to be relatively small with little or no impact on total airflow resistance. ...
The defining feature of asthma is loss of normal post-natal homeostatic control of airways smooth muscle (ASM). This is the key feature that distinguishes asthma from all other forms of respiratory disease. Failure to focus on impaired ASM homeostasis largely explains our failure to find a cure and contributes to the widespread excessive morbidity associated with the condition despite the presence of effective therapies. The mechanisms responsible for destabilizing the normal tight control of ASM and hence airways caliber in post-natal life are unknown but it is clear that atopic inflammation is neither necessary nor sufficient. Loss of homeostasis results in excessive ASM contraction which, in those with poor control, is manifest by variations in airflow resistance over short periods of time. During viral exacerbations, the ability to respond to bronchodilators is partially or almost completely lost, resulting in ASM being “locked down” in a contracted state. Corticosteroids appear to restore normal or near normal homeostasis in those with poor control and restore bronchodilator responsiveness during exacerbations. The mechanism of action of corticosteroids is unknown and the assumption that their action is solely due to “anti-inflammatory” effects needs to be challenged. ASM, in evolutionary terms, dates to the earliest land dwelling creatures that required muscle to empty primitive lungs. ASM appears very early in embryonic development and active peristalsis is essential for the formation of the lungs. However, in post-natal life its only role appears to be to maintain airways in a configuration that minimizes resistance to airflow and dead space. In health, significant constriction is actively prevented, presumably through classic negative feedback loops. Disruption of this robust homeostatic control can develop at any age and results in asthma. In order to develop a cure, we need to move from our current focus on immunology and inflammatory pathways to work that will lead to an understanding of the mechanisms that contribute to ASM stability in health and how this is disrupted to cause asthma. This requires a radical change in the focus of most of “asthma research.”
... The ribs and intercostal muscles form a set of skeletal lever systems that convert intercostal muscle shortening into lateral and cranial motion of the ribs. This costal aspiration system appears to be the primitive ventilation mechanism for amniotes (Brainerd and Owerkowicz, 2006). Accessory diaphragm-like arrangements have evolved independently in mammals, turtles and crocodilians, but in all extant amniotes except turtles, rib motions contribute to lung ventilation, suggesting that costal aspiration is primitive for amniotes (Brainerd, 2015;Brainerd and Owerkowicz, 2006). ...
... This costal aspiration system appears to be the primitive ventilation mechanism for amniotes (Brainerd and Owerkowicz, 2006). Accessory diaphragm-like arrangements have evolved independently in mammals, turtles and crocodilians, but in all extant amniotes except turtles, rib motions contribute to lung ventilation, suggesting that costal aspiration is primitive for amniotes (Brainerd, 2015;Brainerd and Owerkowicz, 2006). ...
The three-dimensional rotations of ribs during breathing are typically described as bucket-handle rotation about a dorsoventrally-oriented axis, pump-handle rotation about a mediolateral axis, and caliper rotation about a rostrocaudal axis. In amniotes with double-headed ribs, rib motion is constrained primarily to one degree-of-freedom (DOF) rotation about an axis connecting the two rib articulations. However, in Squamata, the ribs are single-headed and the hemispherical costovertebral joints permit rotations with three DOF. In this study we use XROMM to quantify rib rotation during deep breathing in four green iguanas. We found that rib rotation was strongly dominated by bucket-handle rotation, thus exhibiting nearly hinge-like motion, despite the potential for more complex motions. The vertebral and sternal segments of each rib did not deform measurably during breathing, but they did move relative to each other at a thin, cartilaginous intracostal joint. While standing still and breathing deeply, four individual iguanas showed variability in their rib postures, with two breathing around a highly inflated posture, and two breathing around a posture with the ribs folded halfway back. Bucket-handle rotations showed clear rostrocaudal gradients, with rotation increasing from the third cervical to the first or second dorsal rib, and then decreasing again caudally, a pattern that is consistent with the intercostal muscles in the rostral intercostal spaces being the primary drivers of inspiration. The constrained, primarily bucket-handle rotations observed here during breathing do not help explain the evolution of permissive, hemispherical costovertebral joints in squamates from the more constrained, double-headed rib articulations of other amniotes.
... This second system probably originated in support of the branchial pump, which gradually gave way to rib-driven aspirational breathing. This system arose in stem-amniotes and had probably become the dominant of the two systems in early amniotes and stemmammals (Janis and Keller 2001;Brainerd and Owerkowicz 2006). ...
... For snakes, a mechanical constraint on ventilatory motions would be particularly detrimental because they have no accessory ventilation mechanism (e.g. the diaphragm of mammals) and thus rely entirely on motions of their ribs (Brainerd, 2015;Brainerd and Owerkowicz, 2006). A possible solution would be to shift the location of ventilatory rib motions away from the constrained regions and instead use an unencumbered region of their elongate bodies. ...
The evolution of constriction and of large prey ingestion within snakes are key innovations that may explain the remarkable diversity, distribution and ecological scope of this clade, relative to other elongate vertebrates. However, these behaviors may have simultaneously hindered lung ventilation such that early snakes may have had to circumvent these mechanical constraints before those behaviors could evolve. Here, we demonstrate that Boa constrictor can modulate which specific segments of ribs are used to ventilate the lung in response to physically hindered body wall motions. We show that the modular actuation of specific segments of ribs likely results from active recruitment or quiescence of derived accessory musculature. We hypothesize that constriction and large prey ingestion were unlikely to have evolved without modular lung ventilation because of their interference with lung ventilation, high metabolic demands and reliance on sustained lung convection. This study provides a new perspective on snake evolution and suggests that modular lung ventilation evolved during or prior to constriction and large prey ingestion, facilitating snakes' remarkable radiation relative to other elongate vertebrates.
... Constraints at this scale, therefore, are displaced from one structure to another more often than they are eliminated. In tetrapod evolution, for example, respiration transitioned from the head (buccal pumping) to the trunk (costal ventilation), relieving the head of this function by shifting it to the trunk, which is already serving in locomotion (Carrier 1987;Janis and Keller 2001;Brainerd and Owerkowicz 2006;Perry and Carrier 2006;Dial et al. 2015). ...
Multifunctionality is often framed as a core constraint of evolution, yet many evolutionary transitions involve traits taking on additional functions. Mouthbrooding, a form of parental care where offspring develop inside a parent's mouth, increases multifunctionality by adding a major function (reproduction) to a structure already serving other vital functions (feeding and respiration). Despite increasing multifunctionality, mouthbrooding has evolved repeatedly from other forms of parental care in at least seven fish families. We hypothesized that mouthbrooding is more likely to evolve in lineages with feeding adaptations that are already advantageous for mouthbrooding. We tested this hypothesis in Neotropical cichlids, where mouthbrooding has evolved four or five times, largely within winnowing clades, providing several pairwise comparisons between substrate-brooding and mouthbrooding sister taxa. We found that the mouthbrooding transition rate was 15 times higher in winnowing than in nonwinnowing clades and that mouthbrooders and winnowers overlapped substantially in their buccal cavity morphologies, which is where offspring are incubated. Species that exhibit one or both of these behaviors had larger, more curved buccal cavities, while species that exhibit neither behavior had narrow, cylindrical buccal cavities. Given the results we present here, we propose a new conceptual model for the evolution of mouthbrooding, integrating the roles of multifunctional morphology and the environment. We suggest that functional transitions like mouthbrooding offer a different perspective on multifunctionality: increasing constraints in one trait may release them for another, generating new evolutionary opportunities.
... This helps to constrain digital reconstruction of vertebral motion segments and limits the total mobility of the joint relative to other anatomical regions (Molnar et al. 2015;Oliver et al. 2016;Jones et al. 2020). Further, the vertebral column plays an important role in diverse behaviors such as locomotion, breathing, and thermoregulation (Buchholtz 1998;Brainerd and Owerkowicz 2006;Cieri et al. 2020;Carrier 1987;Schilling and Hackert 2006;Schilling 2011). Therefore, understanding the functional implications of vertebral changes is key to understanding numerous evolutionary transitions. ...
Deciphering the biological function of rare or extinct species is key to understanding evolutionary patterns across the tree of life. While soft tissues are vital determinants of joint function, they are rarely available for study. Therefore, extracting functional signals from skeletons, which are more widely available via museum collections, has become a priority for the field of comparative biomechanics. While most work has focused on the limb skeleton, the axial skeleton plays a critical role in body support, respiration, and locomotion, and is therefore of central importance for understanding broad-scale functional evolution. Here, we describe and experimentally validate AutoBend, an automated approach to estimating intervertebral joint function from bony vertebral columns. AutoBend calculates osteological range of motion (oROM) by automatically manipulating digitally articulated vertebrae while incorporating multiple constraints on motion, including both bony intersection and the role of soft tissues by restricting excessive strain in both centrum and zygapophyseal articulations. Using AutoBend and biomechanical data from cadaveric experiments on cats and tegus, we validate important modeling parameters required for oROM estimation, including the degree of zygapophyseal disarticulation, and the location of the center of rotation. Based on our validation, we apply a model with the center of rotation located within the vertebral disc, no joint translation, around 50% strain permitted in both zygapophyses and discs, and a small amount of vertebral intersection permitted. Our approach successfully reconstructs magnitudes and craniocaudal patterns of motion obtained from ex vivo experiments, supporting its potential utility. It also performs better than more typical methods that rely solely on bony intersection, emphasizing the importance of accounting for soft tissues. We estimated the sensitivity of the analyses to vertebral model reconstruction by varying joint spacing, degree of overlap, and the impact of landmark placement. The effect of these factors was small relative to biological variation craniocaudally and between bending directions. Within, we also present a new approach for estimating joint stiffness directly from oROM and morphometric measurements that can successfully reconstruct the craniocaudal patterns, but not magnitudes, derived from experimental data. Together, this work represents a significant step forward for understanding vertebral function in difficult-to-study (e.g., rare or extinct) species, paving the way for a broader understanding of patterns of functional evolution in the axial skeleton.
... In a highly similar fashion to fish and amphibian's buccal pumping for breathing, the gular cavity expands by retracting and depressing the hyobranchial skeleton to assist in inspiration. The addition of this non-conflicting motor program allows these lizards to draw more than two times the air volume than available through costal inspiration alone (Brainerd and Owerkowicz, 2006). ...
Feeding and breathing are two functions vital to the survival of all vertebrate species. Throughout the evolution, vertebrates living in different environments have evolved drastically different modes of feeding and breathing through utilizing diversified orofacial and pharyngeal (oropharyngeal) muscles. The oropharyngeal structures are controlled by hindbrain neural circuits. The developing hindbrain shares strikingly conserved organizations and gene expression patterns across vertebrates, thus begs the question of how a highly conserved hindbrain generates circuits subserving diverse feeding/breathing patterns. In this review, we summarize major modes of feeding and breathing and principles underlying their coordination in many vertebrate species. We provide a hypothesis for the existence of a common hindbrain circuit at the phylotypic embryonic stage controlling oropharyngeal movements that is shared across vertebrate species; and reconfiguration and repurposing of this conserved circuit give rise to more complex behaviors in adult higher vertebrates.SIGNIFICANCE STATEMENTUnderstanding how a highly conserved hindbrain generates diverse feeding/breathing patterns is important for elucidating neural mechanisms underlying the execution and coordination of these two vital behaviors. Here, we first briefly summarize key modes of vertebrates feeding/breathing, discuss main principles coordinating feeding/breathing, and provide a unifying hypothesis for the existence of a shared oropharyngeal movement control circuit across species. By synthesizing behavior, structural and neural mechanisms for feeding/breathing functions across evolution, we believe that this review and our hypothesis can open new research avenues for elucidating the precise hindbrain circuits controlling feeding, breathing and other oropharyngeal functions.
... The positioning of the palatal valve appears to influence the acoustic parameters of crocodylian vocalizations: juvenile distress calls emitted with an opened palatal valve are high frequency, high intensity "screeches" compared with the lower frequency "moans" that are emitted while the palatal valve is closed [155]. Further, the volume enclosed within the esophagopharyngeal space can be modulated by movement of the hyoid apparatus during a behavior called "gular pumping" that influences respiration in several reptile lineages [156], and may be relevant for sound production in extant archosaurs [12,157]. A modeling study demonstrated that the frequency modulation needed to produce alligator calls could be achieved by combined tuning of laryngeal subglottal pressure and adduction of the vocal folds [12], which suggests that complex, active motor control patterns are involved in crocodylian vocalization although physiological data are still lacking. ...
Although comprising a paraphyletic assemblage, tuatara, turtles, snakes, lizards, and crocodylians are colloquially grouped as reptiles. These groups all have at least some auditory capabilities but generally do not have very complex vocalizations. Most commonly, the sounds produced by reptiles are associated with defensive or aggressive behavior. Crocodylians and some lizards are the exception, using vocal communication to mediate group cohesion, parental care, courtship, and territoriality. Because of the diversity of acoustic signals and the variety of habitats in which these animals live, coupled with the relatively limited body of literature on reptile bioacoustics, reptiles represent a compelling subject for future studies on the evolution of vocalization.
... Each peak represents elevation of the buccal floor, and each valley represents its depression. The small peaks illustrate buccal oscillation (sensu Brainerd and Owerkowicz 2006) during which air is drawn into the buccal cavity through the nostrils (buccal floor depression) and is pumped out again (buccal floor elevation) through the nostrils without entering the lungs. By contrast, each large peak illustrates breathing during which the pronounced upward movement of the buccal floor presses air into the lungs. ...
Synopsis
In frogs and salamanders, movements of the eyeballs in association with an open palate have often been proposed to play a functional role in lung breathing. In this “palatal buccal pump,” the eyeballs are elevated during the lowering of the buccal floor to suck air in through the nares, and the eyeballs are lowered during elevation of the buccal floor to help press air into the lungs. Here, we used X-Ray Reconstruction of Moving Morphology to investigate eye movements during lung breathing and feeding in bullfrogs and axolotls. Our data do not show eye movements that would be in accordance with the palatal buccal pump. On the contrary, there is a small passive elevation of the eyeballs when the buccal floor is raised. Inward drawing of the eyeballs occurs only during body motion and for prey transport in bullfrogs, but this was not observed in axolotls. Each eye movement in bullfrogs has a vertical, a mediolateral, and an anteroposterior component. Considering the surprisingly weak posterior motion component of the eyeballs, their main role in prey transport might be fixing the prey by pressing it against the buccal floor. The retraction of the buccal floor would then contribute to the posterior push of the prey. Because our study provides no evidence for a palatal buccal pump in frogs and salamanders, there is also no experimental support for the idea of a palatal buccal pump in extinct temnospondyl amphibians, in contrast to earlier suggestions.
... Both birds and crocodilians use costal aspiration-changes in the volume of the ribcage driven by rib motions and the axial musculature-to ventilate their lungs [58]. In both groups, the ribs are bicapitate and form two distinct articulations with the ribcage: the capitulum-parapophysis and tuberculum-diapophysis [53,59]. ...
The Archosauria are a highly successful group of vertebrates, and their evolution is marked by the appearance of diverse respiratory and metabolic strategies. This review examines respiratory function in living and fossil archosaurs, focusing on the anatomy and biomechanics of the respiratory system, and their physiological consequences. The first archosaurs shared a heterogeneously partitioned parabronchial lung with unidirectional air flow; from this common ancestral lung morphology, we trace the diverging respiratory designs of bird- and crocodilian-line archosaurs. We review the latest evidence of osteological correlates for lung structure and the presence and distribution of accessory air sacs, with a focus on the evolution of the avian lung-air sac system and the functional separation of gas exchange and ventilation. In addition, we discuss the evolution of ventilation mechanics across archosaurs, citing new biomechanical data from extant taxa and how this informs our reconstructions of fossils. This improved understanding of respiratory form and function should help to reconstruct key physiological parameters in fossil taxa. We highlight key events in archosaur evolution where respiratory physiology likely played a major role, such as their radiation at a time of relative hypoxia following the Permo-Triassic mass extinction, and their evolution of elevated metabolic rates.
This article is part of the theme issue ‘Vertebrate palaeophysiology’.
... Brainerd and Owerkowicz (2006) discuss a variation of the buccal pump theory, which explains gular pumping in tetrapods. It's status as a distinct theory, the gular pump theory, is undetermined. ...
In the ongoing philosophical debates between scientific realists and antirealists, scientific modeling
is often taken as an exemplar antirealist scientific methodology due to the abstract, idealized,
and metaphorical nature of most scientific models. I argue against the antirealist view and in
favor of a realist view of scientific modeling as it is performed in biological morphology. On my
view, morphological modeling is a type of what I call multiperspectival modeling, which involves
multiple related models deployed to represent a single target phenomenon. I show how
multiperspectival morphological modeling can be incorporated into the version of scientific
realism developed by Richard Boyd, known as accommodationism, based on the role modeling
plays in informing the definitions of natural kind terms and on the role theoretical judgments
play in model construction and deployment. I claim that multiperspectival morphological models
contribute to the inductive and explanatory successes of biological morphology by playing a
central role in accommodating (on the one hand) the inferential, conceptual, and classificatory
practices of morphology to (on the other hand) independently existing causal phenomena. I
intend for the realist view of morphological models presented here to serve as an example for
how scientific modeling can be interpreted realistically across scientific disciplines.
... As aerobic capacity increased throughout tetrapod evolution (Bennett, 1978), greater demands were placed on the respiratory system to eliminate larger quantities of CO 2 (Hedrick et al., 2015;Hillman et al., 2013). Anatomical changes in the production of air flow (i.e., buccal vs. aspiration pump), locomotor posture, accessory breathing muscles, and respiratory-locomotor coupling (Brainerd and Owerkowicz, 2006) would have improved CO 2 release. I propose that neural mechanisms underlying the "metabolic ventilatory drive" would have been critical to connect these mechanical modifications to increased ventilation rates for CO 2 elimination. ...
Haldane and Priestley (1905) discovered that the ventilatory control system is highly sensitive to CO2. This “CO2 chemoreflex” has been interpreted to dominate control of resting arterial PCO2/pH (PaCO2/pHa) by monitoring PaCO2/pHa and altering ventilation through negative feedback. However, PaCO2/pHa varies little in mammals as ventilation tightly couples to metabolic demands, which may minimize chemoreflex control of PaCO2. The purpose of this synthesis is to (1) interpret data from experimental models with meager CO2 chemoreflexes to infer their role in ventilatory control of steady-state PaCO2, and (2) identify physiological causes of respiratory acidosis occurring normally across vertebrate classes. Interestingly, multiple rodent and amphibian models with minimal/absent CO2 chemoreflexes exhibit normal ventilation, gas exchange, and PaCO2/pHa. The chemoreflex, therefore, plays at most a minor role in ventilatory control at rest; however, the chemoreflex may be critical for recovering PaCO2 following acute respiratory acidosis induced by breath-holding and activity in many ectothermic vertebrates. An apparently small role for CO2 feedback in the genesis of normal breathing contradicts the prevailing view that central CO2/pH chemoreceptors increased in importance throughout vertebrate evolution. Since the CO2 chemoreflex contributes minimally to resting ventilation, these CO2 chemoreceptors may have instead decreased importance throughout tetrapod evolution, particularly with the onset and refinement of neural innovations that improved the matching of ventilation to tissue metabolic demands. This distinct and elusive “metabolic ventilatory drive” likely underlies steady-state PaCO2 in air-breathers. Uncovering the mechanisms and evolution of the metabolic ventilatory drive presents a challenge to clinically-oriented and comparative respiratory physiologists alike.
... Buccal pumping, where the floor of the mouth is lowered and air is sucked into the oral cavity and subsequently actively forced into the lungs by elevation of the buccal floor, is a ventilatory mechanism best known in amphibians. [54][55][56] This mode of breathing, however, appears highly unlikely for caseids, due to their tiny head. Several such gulps would have been necessary just to overcome the dead space, which approaches almost 2 L in our caseian reconstruction. ...
The origin of the diaphragm remains a poorly understood yet crucial step in the evolution of terrestrial vertebrates, as this unique structure serves as the main respiratory motor for mammals. Here, we analyze the paleobiology and the respiratory apparatus of one of the oldest lineages of mammal-like reptiles: the Caseidae. Combining quantitative bone histology and functional morphological and physiological modeling approaches, we deduce a scenario in which an auxiliary ventilatory structure was present in these early synapsids. Crucial to this hypothesis are indications that at least the phylogenetically advanced caseids might not have been primarily terrestrial but rather were bound to a predominantly aquatic life. Such a lifestyle would have resulted in severe constraints on their ventilatory system, which consequently would have had to cope with diving-related problems. Our modeling of breathing parameters revealed that these caseids were capable of only limited costal breathing and, if aquatic, must have employed some auxiliary ventilatory mechanism to quickly meet their oxygen demand upon surfacing. Given caseids' phylogenetic position at the base of Synapsida and under this aquatic scenario, it would be most parsimonious to assume that a homologue of the mammalian diaphragm had already evolved about 50 Ma earlier than previously assumed.
... E xtant amniotes (the clade comprising mammals, turtles, birds, crocodilians and lepidosaurs) ventilate their lungs using a diversity of mechanisms (Fig. 1a). The most common of these solutions involves expansion and contraction of the ribcage effected by the intercostal muscles, either primarily, as in lepidosaurs (squamates and tuataras) or to supplement previously accessory structures that eventually became primary (for example, mammalian diaphragm) 1,2 . Costal ventilation is impossible in turtles because their intercostal muscles are lost during embryogenesis 3 and their ribs are bound in a typically rigid shell 4 . ...
Background. The turtle body plan differs markedly from that of other vertebrates and serves as a model system for studying structural and developmental evolution. Incorporation of the ribs into the iconic turtle shell negates the rib movements that effect lung ventilation in the majority of air-breathing amniotes (the clade encompassing mammals, lizards, turtles, birds, and crocodilians). Instead, turtles have a novel abdominal-muscle-based ventilatory apparatus whose evolutionary origin remains a mystery. Methods. Here we show through broadly comparative anatomical and histological analyses that the earliest stem-group turtle form the middle Permian (260 mya), Eunotosaurus africanus, has several turtle-specific lung ventilation characters: rigid ribcage, inferred loss of intercostal muscles which drive costal ventilation in all other amniotes, and histological correlates for the primary muscle, M. transverses, used in exhalation. Results. Our results place the origin of the unique lung ventilatory apparatus of extant turtles shortly after the divergence of turtles from other reptiles and approximately 50 million years before the oldest known fully developed shell. Discussion. These data indicate that it was an easing of structural constraints through division of function (divergent specialization) between the ribs and abdominal musculature that facilitated the evolution of both the novel turtle lung ventilation mechanism and the turtle shell.
... For example, based on the early development of outgrowth of membrane bone from the ribs of extant turtles (e.g.,[38]), the model predicts that earlier stem turtles had slightly broadened ribs with some intramembranous outgrowth of bone from the perichondral/periosteal collar of the rib. Based on the inference that the unique abdominal muscle ventilation system of turtles[44], in which the muscles attach to the ventral portion of the carapace[45], arose from a basal amniote with costal ventilation[46], the model also predicts that early stem turtles likely had both intercostal muscles (unlike Eunotosaurus) and muscles beginning to insert on the ventral side of the trunk/dorsal ribs. Histological data for Milleretta rubidgei has yet to be obtained, but this moderately broad-ribbed species, inferred in phylogenetic analyses to have diverged from the turtle stem earlier than Eunotosaurus[11,30,47], meets many of these morphological predictions (Figure 4). ...
... By contrast, amniotes largely abandoned cutaneous respiration. They fill and empty their larger, more complex lungs primarily by moving their ribs to alter the pressure within the thoracic cavity (Brainerd and Owerkowicz, 2006). Present-day amniotes comprise six monophyletic groups or clades: mammals (Mammalia), turtles (Testudines), the tuatara (Rhynchocephalia), lizards and snakes (Squamata), crocodylians (Crocodylia), and birds (Aves) (Gauthier et al., 1988). ...
Amniotes have been the most diverse and successful group of land vertebrates. They attained a global distribution and are found everywhere except in the deepest realms of the ocean. Amniotes repeatedly and successfully invaded the seas and took to the air. All amniotes share the possession of the amniotic (cleidoic) egg, which freed them from dependence on water for reproduction. Current research distinguishes two major lineages among amniotes: Synapsida (mammals and their extinct close relatives) and Reptilia. The most diverse group of reptiles is Diapsida (turtles, lizards, snakes, tuatara, crocodylians, birds, and many extinct groups).
... Accessory breathing mechanisms, derived musculoskeletal systems that lower the energetic cost of lung ventilation or increase the potential for gas exchange, occur throughout Tetrapoda (e.g., Owerkowicz et al. 1999;Farmer and Carrier 2000;Claessens 2004aClaessens , 2004bCodd et al. 2005;Brainerd and Owerkowicz 2006). Four of the anatomical systems that have evolved respiratory functions in specific archosaur clades are discussed below: costal processes, the pelvis, the diaphragmaticus muscle, and the gastralial apparatus. ...
... Active expiration in mammals, like lung/priming burst complexes, is strongly recruited by chemosensory activation (Burke et al., 2015). Further, in salamanders, which likely resemble the earliest amphibians, flank muscles are recruited for forced expiration, supplementing the buccal pump (Brainerd, 1994(Brainerd, , 1998Brainerd and Owerkowicz, 2006). Thus, in early air-breathing vertebrates we speculate that the buccal oscillator in r7/8 driving the buccal pump was the first burst generator involved in lung inflation but was likely soon to be supplemented by a burst generators for active expiration, equivalent to the priming area in frogs, located in r4-6. ...
... Another source of constraint is the conflicting functions of animal phenotypes (Higham & Irschick 2013). This is the case for breathing and running in some lizards, where hypaxial and epaxial muscles drive both the movements of the ribs (for breathing) and of the body (for locomotion) (Carrier 1991;Farmer & Carrier 2000a, b;Brainerd & Owerkowicz 2006). The dual role of these muscles would appear to be one important factor that can limit the endurance capacity of a lizard, and therefore its escape ability in some situations. ...
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
Unlike the majority of sauropsids, which breathe primarily through costal and abdominal muscle contractions, extant crocodilians have evolved the hepatic piston pump, a unique additional ventilatory mechanism powered by the diaphragmaticus muscle. This muscle originates from the bony pelvis, wrapping around the abdominal viscera, extending cranially to the liver. The liver then attaches to the caudal margin of the lungs, resulting in a sub-fusiform morphology for the entire “pulmo-hepatic-diaphragmatic” structure. When the diaphragmaticus muscle contracts during inspiration, the liver is pulled caudally, lowering pressure in the thoracolumbar cavity, and inflating the lungs. It has been established that the hepatic piston pump requires the liver to be displaced to ventilate the lungs, but it has not been determined if the lungs are freely mobile or if the pleural tissues stretch ventrally. It has been hypothesized that the lungs are able to slide craniocaudally with the liver due to the smooth internal ceiling of the thoracolumbar cavity. We assess this through ultrasound video and demonstrate quantitatively and qualitatively that the pulmonary tissues are sliding craniocaudally across the interior thoracolumbar ceiling in actively ventilating live juvenile, sub-adult, and adult individuals ( n = 7) of the American alligator ( Alligator mississippiensis ) during both natural and induced ventilation. The hepatic piston is a novel ventilatory mechanism with a relatively unknown evolutionary history. Questions related to when and under what conditions the hepatic piston first evolved have previously been left unanswered due to a lack fossilized evidence for its presence or absence. By functionally correlating specific characters in the axial skeleton to the hepatic piston, these osteological correlates can be applied to fossil taxa to reconstruct the evolution of the hepatic piston in extinct crocodylomorph archosaurs.
The rapidly changing ecological situation implies a high level of adaptation capabilities of the animal organism to the realities of the environment. In the conditions of animal husbandry, this is possible only with regular monitoring of the morphological state of organs and systems, especially the respiratory system, which is actively influenced by the features of housing, atmospheric air, feeding, as well as the medical and preventive measures that are carried out. Therefore, the functioning of the lungs as an open morphofunctional system directly depends on the nature of their dynamic interaction with a complex complex of physical and chemical environmental factors. In this regard, there is an obvious need for a detailed study of the macro- and micromorphology of the respiratory organs, since such organs are a system by which the body "builds itself from environmental conditions". It is also necessary to take into account that this system occupies one of the leading positions in ensuring the optimal level of functioning of the body, since the animal's development, metabolic processes, and its state of health largely depend on its work. Establishing the macro- and micromorphological features of the respiratory system is the foundation for preventive and therapeutic measures. The respiratory system ensures the intake of oxygen into the body and the excretion of carbon dioxide from it, and the gas exchange between blood and air. The scientific article is devoted to the study of the macro- and micromorphological features of the lungs of a sexually mature horse - Equus Feruscaballus L., 1758. With the help of anatomical preparation and macroscopic, histological, morphometric and statistical methods of research, the morphology of the lungs was investigated and their belonging to a certain anatomical type was determined. As a result of the research, the partial structure of the lungs was determined, their topography, shape, dimensions, branching of the bronchi of the bronchial tree, results of organometry (absolute and relative lung mass), morphometric assessment of their morphological structures, asymmetry coefficient, etc. were determined. According to the results of morphological studies, the characteristic morphological features of the macro- and microscopic structure of the lungs of a mature horse were revealed according to the class, age and species of animals. The presence of individual morphological features in the lobular structure of the lungs of horses was revealed. In particular, there are only two lobes in the left lung (cranial and caudal), and three lobes in the right lung (cranial, caudal and additional). The alveolar tree of the lungs of horses is shortened, wide and has a vesicular structure. The conducted research to a certain extent expands and supplements information about the species, breed and morphological features of the anatomical and histological structure of the lungs in domestic animals and is important for assessing the clinical and morphological state of animals in normal conditions and for identifying the pathogenesis of animal diseases related to the respiratory organs.
The skeleton and inferred neurosensory system of the ancestral amniote provide a point of departure to trace neurosensory evolution in extinct stem-mammals that culminated in the origin of crown Mammalia. Early stem-mammal evolution mostly involved enhanced integration of skeletal elements for feeding and locomotion as they became apex predators. With the origin of Cynodontia, modifications of the dentition, oropharynx, and braincase suggest that mastication and olfaction had become major influences in stem-mammal evolution, probably through ontogenetic cascades triggered by expression of an expanded olfactory genome. With the origin of Mammaliaformes, brain size nearly doubled in response to further elaboration of the olfactory system, dentition, the elaboration of hair, all in the context of miniaturization of adult body size. One of the keys to understanding major features in stem-mammal evolution and the origin of Mammalia is the emergence of an unsurpassed ability to perceive and process olfactory and dietary information, and to diversify and exploit the fast-changing chemical environments they faced throughout much of their history. Whether through connectional invasions and epigenetic population matching, or some other developmental mechanism, hypertrophy in peripheral sensory arrays produced cascading influences on central organization. These led to emergence of the unique mammalian neocortex and to the physiological and behavioral repertoires that are so distinctive of mammals today.
The origin of the unique body plan of turtles has long been one of the most intriguing mysteries in evolutionary morphology. Discoveries of several new stem-turtles, together with insights from recent studies on the development of the shell in extant turtles, have provided crucial new information concerning this subject. It is now possible to develop a comprehensive scenario for the sequence of evolutionary changes leading to the formation of the turtle body plan within a phylogenetic framework and evaluate it in light of the ontogenetic development of the shell in extant turtles. The fossil record demonstrates that the evolution of the turtle shell took place over millions of years and involved a number of steps.
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
The structure of the lung subserves its function, which is primarily gas exchange, and selection for expanded capacities for gas exchange is self-evident in the great diversity of pulmonary morphologies observed in different vertebrate lineages. However, expansion of aerobic capacities does not explain all of this diversity, leaving the functional underpinnings of some of the most fascinating transformations of the vertebrate lung unknown. One of these transformations is the evolution of highly branched conducting airways, particularly those of birds and mammals. Birds have an extraordinarily complex circuit of airways through which air flows in the same direction during both inspiration and expiration, unidirectional flow. Mammals also have an elaborate system of conducting airways; however, the tubes arborize rather than form a circuit, and airflow is tidal along the branches of the bronchial tree. The discovery of unidirectional airflow in crocodilians and lizards indicates that several inveterate hypotheses for the selective drivers of this trait cannot be correct. Neither endothermy nor athleticism drove the evolution of unidirectional flow. These discoveries open an uncharted area for research into selective underpinning of unidirectional airflow.
Background. The turtle body plan differs markedly from that of other vertebrates and serves as a model system for studying structural and developmental evolution. Incorporation of the ribs into the iconic turtle shell negates the rib movements that effect lung ventilation in the majority of air-breathing amniotes (the clade encompassing mammals, lizards, turtles, birds, and crocodilians). Instead, turtles have a novel abdominal-muscle-based ventilatory apparatus whose evolutionary origin remains a mystery. Methods. Here we show through broadly comparative anatomical and histological analyses that the earliest stem-group turtle form the middle Permian (260 mya), Eunotosaurus africanus, has several turtle-specific lung ventilation characters: rigid ribcage, inferred loss of intercostal muscles which drive costal ventilation in all other amniotes, and histological correlates for the primary muscle, M. transverses, used in exhalation. Results. Our results place the origin of the unique lung ventilatory apparatus of extant turtles shortly after the divergence of turtles from other reptiles and approximately 50 million years before the oldest known fully developed shell. Discussion. These data indicate that it was an easing of structural constraints through division of function (divergent specialization) between the ribs and abdominal musculature that facilitated the evolution of both the novel turtle lung ventilation mechanism and the turtle shell.
In the solar system and perhaps beyond, when many aspects are considered, Earth is a unique planet. Often called the twin planet to Earth because of its close proximity, its comparable radius/size, and its similar mass and density, the atmosphere of Venus is very different from that of Earth. It comprises 97% carbon dioxide (CO2), 2% nitrogen (N2), and less than 1% molecular oxygen (O2), water (vapor) (H2O), and methane (CH4) (e.g., Ingersoll 2007; Svedhem et al. 2007). Among the planets of the solar system, while the atmosphere of Earth now contains only a small amount of CO2, those of Venus and Mars contain ~96.5 and ~98% of it, respectively. The atmospheres of Jupiter and Saturn, two of the four solar system’s gas giant (also called Jovian) planets, consist mostly of hydrogen (H2) and helium (He) (e.g., Lissauer and Stevenson 2006), while Mercury has a very thin and highly variable atmosphere containing H2, He, O2, Sodium (Na), calcium (Ca), potassium (K), and water vapor with a combined pressure level of ~10−14 bar (1 nPa) (Domingue et al. 2007; McClintock et al. 2008). The most important factors that sanctioned the realization of the so-called “carbon-based life” on Earth include (a) an atmosphere rich in O2, (b) a biological range of temperature and the presence of water (the much acclaimed “universal solvent”) in the three states of matter – solid (ice), liquid (water), and gas (water vapor), and (c) a magnitude of gravity sufficient to prevent the loss of most of the atmospheric gases to the outer space, including hydrogen (H), the smallest atom, without wielding too much pressure on delicate biological life.
Reconstruction of the changes that have occurred during the evolution of the gas exchangers is riddled with pitfalls. This is mainly because of the almost complete lack of instructive fossilized materials, as would be expected, of soft tissues such as the respiratory organs/structures. The precept that “progeny recapitulates phylogeny” is too simple for the discipline of evolutionary developmental biology (evo–devo) to be directly extrapolated in studies of the paleobiology of respiration (e.g., Northcutt 1990). For example, during their development (metamorphosis), amphibians undergo drastic changes in the form, location, and function of the gas exchangers (Sect. 5.4.1). The transformations cannot be predicted from one level of development to another. Moreover, respiration appears to be too important for perpetuation of “primitive” features from one evolutionary level to another.
Increased organismic complexity in metazoans was achieved via the specialization of certain parts of the body involved in different faculties (structure-function complexes). One of the most basic metabolic demands of animals in general is a sufficient supply of all tissues with oxygen. Specialized structures for gas exchange (and transport) consequently evolved many times and in great variety among bilaterians. This review focuses on some of the latest advancements that morphological research has added to our understanding of how the respiratory apparatus of the primarily terrestrial vertebrates (amniotes) works and how it evolved. Two main components of the respiratory apparatus, the lungs as the "exchanger" and the ventilatory apparatus as the "active pump," are the focus of this paper. Specific questions related to the exchanger concern the structure of the lungs of the first amniotes and the efficiency of structurally simple snake lungs in health and disease, as well as secondary functions of the lungs in heat exchange during the evolution of sauropod dinosaurs. With regard to the active pump, I discuss how the unique ventilatory mechanism of turtles evolved and how understanding the avian ventilatory strategy affects animal welfare issues in the poultry industry.
Introduction Air-breathing vertebrates constitute a large group of diverse animals belonging to different taxonomic classes. Air breathing evolved independently in different groups of fish and early tetrapods, and extant species employ an array of different air-breathing organs that are derived from various existing structures, such as the gastrointestinal tract or the buccopharyngeal cavity (see Chapter 6). True lungs in terrestrial vertebrates develop embryologically as a ventral outpocketing of the posterior pharynx into a paired structure that extends into the peritoneal cavity. The entrance to the lung through the pharynx is guarded by the glottis, and the lungs are perfused by a pulmonary artery that carries oxygen-poor blood to the respiratory surfaces in the lungs, while a pulmonary vein returns oxygen-rich blood to the heart. Although the lungs of extant air-breathing vertebrates share a common embryological development and overall arrangement, there are large structural differences, from the simple sac-like lungs of amphibians to the complex structure of the alveolar lungs of mammals and the parabronchial lungs of birds. Regardless of the structural variation, in all air-breathing vertebrates the gas-exchange organs provide adequate exchange of O and CO2 to meet the variable metabolic needs of the animal. Vertebrates supply the majority of their energetic requirements through aerobic metabolism. As the product of aerobic metabolism, adenosine triphospate (ATP), cannot be effectively stored, the oxygen-transport process represents a continual balance between delivery of oxygen (supply) and the use of ATP (demand).
When a predator attacks, prey are faced with a series of 'if', 'when' and 'how' escape decisions – these critical questions are the foci of this book. Cooper and Blumstein bring together a balance of theory and empirical research to summarise over fifty years of scattered research and benchmark current thinking in the rapidly expanding literature on the behavioural ecology of escaping. The book consolidates current and new behaviour models with taxonomically divided empirical chapters that demonstrate the application of escape theory to different groups. The chapters integrate behaviour with physiology, genetics and evolution to lead the reader through the complex decisions faced by prey during a predator attack, examining how these decisions interact with life history and individual variation. The chapter on best practice field methodology and the ideas for future research presented throughout, ensure this volume is practical as well as informative.
The key difference between amniotes (reptiles, birds and mammals) and anamniotes (amphibians in the broadest sense of the word) is usually considered to be the amniotic egg, or a skin impermeable to water. We propose that the change in the mode of lung ventilation from buccal pumping to costal (rib-based) ventilation was equally, if not more important, in the evolution of tetrapod independence from the water. Costal ventilation would enable superior loss of carbon dioxide via the lungs: Only then could cutaneous respiration be abandoned and the skin made impermeable to water. Additionally efficient carbon dioxide loss might be essential for the greater level of activity of amniotes. We examine aspects of the morphology of the heads, necks and ribs that correlate with the mode of ventilation. Anamniotes, living and fossil, have relatively broad heads and short necks, correlating with buccal pumping, and have immobile ribs. In contrast, amniotes have narrower, deeper heads, may have longer necks, and have mobile ribs, in correlation with costal ventilation. The stem amniote Diadectes is more like true amniotes in most respects, and we propose that the changes in the mode of ventilation occurred in a stepwise fashion among the stem amniotes. We also argue that the change in ventilatory mode in amniotes related to changes in the postural role of the epaxial muscles, and can be correlated with the evolution of herbivory.
We used electromyography (EMG) to determine whether the terrestrial caecilian Dermophis mexicanus uses hypaxial muscle to assist in exhalation. During inhalation D. mexicanus generates high body cavity pressures using a buccal pump. Previous workers have hypothesized that exhalation is passive, occurring when high pressure air in the lung moves to the lower pressure atmosphere when the glottis is opened. This passive exhalation mechanism contrasts with other amphibians which have been shown to use hypaxial muscle to assist in exhalation. In this study, we implanted EMG electrodes on the transverse abdominis (TA) muscle of two caecilians to record muscle activity during exhalation. We observed no EMG activity from the TA muscle during exhalation, confirming that D. mexicanus uses a passive exhalation mechanism.
The haemodynamics of the anatomically undivided ventricle of the monitor lizard Varanus exanthematicus have been examined by measurements of blood pressure and flow. Central blood , and pH were also measured.
Intracardiac pressure measurements show the ventricle to be functionally divided throughout systole into a high pressure pump (cavum arteriosum : ‘mean’ pressure 89 cm H2O) perfusing the systemic circulation, and a low pressure pump (cavum pulmonale: ‘mean’ pressure 40 cm H2O) perfusing the pulmonary circulation. Hypoxia produced by asphyxia or N2 breathing changed systolic pressures in the ventricular cava, but never resulted in superimposable pressure waveforms which would have indicated a break-down from ventricular division into two pressure pumps. Diastolic pressures were superimposable in the ventricular cava under all conditions.
Analysis of blood and O2 content revealed the potential for nearly complete separation of left and right atrial blood in the ventricle, but both left-to-right and right-to-left shunts of considerable magnitude could also develop.
The varanid heart with its systolic pressure separation allows the development of high blood pressure gradients capable of driving a large cardiac output through the high impedance systemic vascular beds. Concurrently, the low impedance pulmonary circuit is perfused at a much reduced blood pressure, circumventing filtration of plasma into the lungs and impairment of gas exchange. Haemodynamically this situation resembles that present in crocodilians and the homeothermic vertebrates.
Squamate reptiles rely heavily on two nasal chemical senses in directing most of their behavior: nasal olfaction and vomeronasal function. For most behaviors in most species, the vomeronasal system is the predominant sense. It has been suggested, however, that geckos are unusual in the extent to which they rely on nasal olfaction rather than vomeronasal function. In this study, we use defensive tail display as a behavioral bioassay to examine the context and relative use of olfaction vs. vomeronasal function in a eublepharid gecko, Coleonyx brevis. When presented with appropriate snake-predator skin chemicals in the absence of relevant visual stimuli, C. brevis exhibits a defensive tail display that has been shown to be adaptive in defending against snake predators. We demonstrate that olfactory cues alone are sufficient to provoke the behavior and that geckos precede the display in many cases with “buccal pulsing,” a behavior that we suggest is an olfactory sampling mechanism analogous to mammalian sniffing. Our results support the gecko-olfaction hypothesis and demonstrate that geckos use nasal olfaction to discriminate among potential predator species. We discuss alternative hypotheses for the origin of species-specific, chemosensory predator identification in Coleonyx. © 1996 Wiley-Liss, Inc.
Endothermic tetrapods differ dramatically from ectothermic tetrapods in having a great capacity to sustain vigorous locomotion. This difference reflects alternative adaptive responses to a mechanical constraint that was an inherent consequence of the vertebrate transition from aquatic to terrestrial modes of locomotion and respiration. The earliest tetrapods may not have been able to walk and breathe at the same time. Their sprawling gait and lateral vertebral bending would have required unilateral contractions of the thoracic musculature that may have interfered with the bilateral movements necessary for breathing. Modern lizards provide support for this hypothesis because their breathing is greatly reduced during locomotor activity. Tetrapod lineages that gave rise to modern ectotherms apparently retained this constraint. The lineages from which birds and mammals are derived have undergone morphological changes that enable simultaneous running and breathing. In modern tetrapods upright posture is correlated with endothermic metabolism. This correlation may have arisen to circimvent ancestral constraints on locomotor stamina.-from Author
Functional analysis of lung ventilation in salamanders combined with historical analysis of respiratory pumps provides new perspectives on the evolution of breathing mechanisms in vertebrates. Lung ventilation in the aquatic salamander Necturus maculosus was examined by means of cineradiography, measurement of buccal and pleuroperitoneal cavity pressures, and electromyography of hypaxial musculature. In deoxygenated water Necturus periodically rises to the surface, opens its mouth, expands its buccal cavity to draw in fresh air, exhales air from the lungs, closes its mouth, and then compresses its buccal cavity and pumps air into the lungs. Thus Necturus produces only two buccal movements per breath: one expansion and one compression. Necturus shares the use of this two-stroke buccal pump with lungfishes, frogs and other salamanders. The ubiquitous use of this system by basal sarcopterygians is evidence that a two-stroke buccal pump is the primitive lung ventilation mechanism for sarcopterygian vertebrates. In contrast, basal actinopterygian fishes use a four-stroke buccal pump. In these fishes the buccal cavity expands to fill with expired air, compresses to expel the pulmonary air, expands to fill with fresh air, and then compresses for a second time to pump air into the lungs. Whether the sarcopterygian two-stroke buccal pump and the actinopterygian four-stroke buccal pump arose independently, whether both are derived from a single, primitive osteichthyian breathing mechanism, or whether one might be the primitive pattern and the other derived, cannot be determined.
Gastralia are dermal ossifications situated in the ventral abdominal wall. Gastralia may be plesiomorphic for tetrapods, but are only retained in extant Crocodylia and Sphenodon, and possibly as part of the chelonian plastron. In contrast to previously published reports, a similar structural configuration of the gastralia is shared throughout prosauropods and (non-ornithurine) theropods. Within the Prosauropoda and Theropoda, the gastralial system consists of approximately 8 to 21 metamerie rows. Each row consists of four bones: two lateral and two medial rods. Gastralia of the cranialmost or caudalmost rows may coalesce, forming a median chevron-shaped gastralium. The lateral gastralia articulate in parallel with the medial gastralia in an elongated groove. The medial gastralia imbricate with contralateral gastralia along the ventral midline, creating a series of cranially directed chevrons. Thus all the gastralia are connected to one another, and operate as a single functional unit. The bones recently identified as sauropod gastralia show no morphological similarities with the gastralia of prosauropods and theropods and are probably sternal elements. No gastralia have been recovered in the Ornithischia.In contrast to the reduction of the gastralia in other amniote groups, theropod gastralia show elaborate modification. The anatomy of the gastralial system indicates a more active function than abdominal support or protection. The gastralia may have affected the shape and volume of the trunk in theropods, and may have functioned as an accessory component of the aspiration pump, increasing tidal volume. Moreover, if the caudal region of the lungs in some theropods had differentiated to form abdominal air-sacs, the gastralia might have ventilated them. Gastralial aspiration may have been linked to the generation of small pressure differences between potential cranial and caudal lung diverticula, which may have been important for the evolution of the unidirectional airflow lung of birds.
Movements of the pelvic girdle have recently been found to contribute to inspiratory airflow in both crocodilians and birds. Although the mechanisms are quite different in birds and crocodilians, participation of the pelvic girdle in the production of inspiration is rare among ver- tebrates. This raises the possibility that the pelvic musculoskeletal system may have played a role in the ventilation of basal archosaurs. Judging from the mechanism of pelvic aspiration in croco- dilians and the structure of gastralia in basal archosaurs, we suggest that an ischiotruncus muscle pulled the medial aspect of the gastralia caudally, and thereby helped to produce inspiration by increasing the volume of the abdominal cavity. From this basal mechanism, several archosaur lin- eages appear to have evolved specialized gastralia, pelvic kinesis, and/or pelvic mobility. Kinetic pubes appear to have evolved independently in at least two clades of Crocodylomorpha. This con- vergence suggests that a diaphragmatic muscle may be basal for Crocodylomorpha. The pelvis of pterosaurs was long, open ventrally, and had prepubic elements that resembled the pubic bones of Recent crocodilians. These characters suggest convergence on the pelvic aspiratory systems of both birds and crocodilians. The derived configuration of the pubis, ischium and gastralia of non-avian theropods appears to have enhanced the basal gastral breathing mechanism. Changes in structure of the pelvic musculoskeletal system that were present in both dromaeosaurs and basal birds may have set the stage for a gradual reduction in the importance of gastral breathing and for the evo- lution of the pelvic aspiration system of Recent birds. Lastly, the structure of the pelvis of some ornithischians appears to have been permissive of pubic and ischial kinesis. Large platelike pre- pubic processes evolved three times in Ornithischia. These plates are suggested to have been in- strumental in an active expansion of the lateral abdominal wall to produce inspiratory flow. Thus, many of the unique features found in the pelvic girdles of various archosaur groups may be related to the function of lung ventilation rather than to locomotion.
The identification and demonstration of an evolutionary constraint is suggested to be a four step process: 1) recognition of a possible mechanism of constraint, 2) formation of an historical scenario of the consequences of the constraint, 3) elucidation of the causal mechanism in the modern analog or model, and 4) phylogenetic correlation of the constraint with theproposed effect in extant lineages. Steps 1 and 2 represent the formation of two interdependenthypotheses, and steps 3 and 4 are tests of those hypotheses.
This approach is illustrated with an example from the musculo-skeletal system of tetrapod vertebrates. Consideration of the anatomy and mode of locomotion of lizards led to the hypothesisthat they may not be able to run and breathe at the same time. Analysis of the pattern of ventilatory airflow of lizards supports this hypothesis. Tidal and minute volume increase above resting levels during slow walking (i.e., speeds below 10% of maximum running speed), but decline rapidly at higher speeds. Furthermore, electromyographic monitoring of the hypaxial muscles indicates a clear conflict between locomotor and ventilatory functions. Key anatomical characters, suggested to be responsible for the conflict, can be traced back to the earliest tetrapods. The organization of the two extant lineages that do breathe while running (i.e., birds andmammals) suggests that the evolution of an ability to breathe during locomotion required modifications of the ancestral configuration that separate locomotor and ventilatory function.
Video and ciné films of mammals running at the trot-gallop transition were analysed to measure breathing frequencies. Breathing frequency at the trot-gallop transition (fb, in Hz) was shown to decrease with increasing body mass (M, in kg) and was described by the equation fb = 5.08 M-0.14. The stiffness of the thorax and diaphragm of mice, rats, rabbits and wallabies was calculated and this, together with the mass of the viscera, was used to calculate the natural frequency of the system (nft, in Hz). The relationship between nft and body mass can be described by the equation nft = 5.02M-0.18. The significance of these results is discussed in relation to models of mechanical linkage between respiratory and locomotory movements.
Ciné film and synchronized records of respiratory flow were obtained from Thoroughbred racehorses cantering on a treadmill at speeds of 9 and 11ms−1.
Horses and some other galloping and hopping mammals link their breathing and locomotion, taking exactly one breath per stride. Three theoretical mechanisms by which the movements of locomotion might drive ventilation are considered.
(i) Flexion of the lumbosacral joint and the resulting forward sweep of the pelvis pushes the viscera against the diaphragm. However, back flexion lags behind ventilation at 11ms−1 and could not exclusively drive ventilation at this speed. (ii) Loading of the thorax by the impact of the forelimbs with the ground might force air out of the lungs. If the respiratory system were damped sufficiently to perform as this mechanism requires, the work of driving ventilation would make up approximately 15 % of the total work of running. In comparison with other estimates of the work of ventilation this seems improbably high, (iii) The observed phase relationship between displacements of the viscera, caused by the accelerations of the body during running, and respiratory airflow is not consistent with a tuned visceral piston mechanism driving breathing.
Thus, it would seem likely that back flexion is likely to contribute towards driving ventilation but loading of the thorax and the visceral piston mechanism do not.
We have observed that birds of several different taxa move their tails in conjunction with sound production. These observations suggested to use that tail movements might also be associated with ventilation. Since we hypothesized that rhythmic movements of the tail and pelvis will ventilate the lungs, the activities of tail, epaxial and cloacal muscles of the pigeon were examined. Electromyograms (EMGs) were recorded from these muscles while ventilation was monitored. A muscle was considered to have ventilatory activity when the EMG activity had an obvious correlation to either inspiration or expiration. To obtain further information about the correlation between muscular activity and ventilation, we induced hyperpnea by administering 5% CO2. We report that the tail muscles that function as expiratory muscles are the M. caudofemoralis, the M. pubocaudalis internus and the M. pubocaudalis externus. We refer to these as the suprapubic abdominal muscles to distinguish them from the infrapubic (ventral) abdominal muscles. These muscles depress the pelvis and the uropygium and compress the thoracoabdominal cavity. M. transversus cloacae functions as an expiratory muscle by protracting the cloaca or by reducing its compliance. Of the suprapubic muscles we studied, the only inspiratory muscle is the axial muscle, M. longissimus dorsi. M. longissimus dorsi acts at the notarial-synsacral junction to elevate the pelvis. The rocking movements of the notarial-synsacral joint appear to be important for ventilation during conditions in which the sternum is 'fixed', such as when the bird is resting on its breast. We suggest that a division of labor may exist between the infra- and suprapubic abdominal muscles during ventilation such as panting or vocalization.
The role that the hypaxial muscles play in locomotion has been largely ignored by biologists. In tetrapods, there are at least three possibilities. First, the hypaxial muscles might bend the trunk laterally to increase stride length. Second, they might stabilize the trunk against the horizontal, lateral and vertical components of the propulsive force. Alternatively, they might not be involved in locomotion. This study evaluated these three hypotheses by analyzing the activity of the hypaxial muscles of green iguanas (Iguana iguana). During walking, the rectus abdominis, obliquus externus superficialis and profundus, intercostales externi, and ventral portion of the intercostales interni on one side of the trunk acted synergistically with the lateral portion of the intercostales interni and obliquus internus on the other side of the trunk. This pattern supports the hypothesis that the hypaxial muscles act to stabilize the trunk during locomotion. Specifically, the longitudinally oriented rectus abdominis, obliquus externus profundus and ventral portion of the intercostales interni appear to stabilize the trunk against the horizontal and lateral components of the propulsive force, which tend to rotate the girdles in the horizontal plane. The obliquely oriented obliquus externus superficialis, intercostales externi, lateral portion of the intercostales interni and obliquus internus appear to stabilize the trunk against the vertical component, which induces long-axis torsion in the trunk. Thus, the demands of locomotion may provide a functional explanation for the basic organization of the hypaxial muscles of tetrapods.
Patterns of muscle activity during lung ventilation, patterns of innervation and some contractile properties were measured in the hypaxial muscles of green iguanas. Electromyography shows that only four hypaxial muscles are involved in breathing. Expiration is produced by two deep hypaxial muscles, the transversalis and the retrahentes costarum. Inspiration is produced by the external and internal intercostal muscles. Although the two intercostal muscles are the main agonists of inspiration, neither is involved in expiration. This conflicts with the widely held notion that the different fibre orientations of the two intercostal muscles determine their ventilatory action.
Several observations indicate that ventilation is produced by slow (i.e. non twitch) fibres of these four muscles. First, electromyographic (EMG) activity recorded from these muscles during ventilation has an unusually low range of frequencies (<100Hz). Such low-frequency signals have been suggested to be characteristic of muscle fibres that do not propagate action potentials (i.e. slow fibres). Second, during inspiration, EMG activity is restricted to the medial sides of the two intercostal muscles. Muscle fibres from this region have multiple motor endplates and exhibit tonic contraction when immersed in saline solutions of high potassium content. Like the intercostals, the transversalis and retrahentes costarum muscles also contain fibres with multiple motor endplates. Thus, although breathing is a phasic activity, it is produced by tonic (i.e. slow) muscle fibres. The intercostal muscles are also involved in postural and locomotor movements of the trunk. However, such movements employ twitch as well as slow fibres of the intercostal muscles.
Ventilation is achieved by, and dependent on, the respiratory muscles. Lung diseases increase the demand for ventilation and thus the load on the respiratory muscles. At the same time gas exchange is impaired and hypoxia may result. In addition the ability of the respiratory muscles to generate force may be impaired, particularly in hyperinflation, by excessive muscle shortening, increased velocity of contraction and changes in chest wall configuration. Such impairment of the respiratory muscle pump may exacerbate hypoxia. Increased work of breathing in severe pulmonary disease may lead to fatigue of the inspiratory muscles, thereby intensifying hypoxia. Hypoxia in turn may impair respiratory muscle function, thereby perpetuating a downward spiral of clinical respiratory failure. Although muscle ischaemia, in which tissue hypoxia, impaired supply of energy substrate, and lactate accumulation all occur, is known to predispose to fatigue, there is little information on the effects of hypoxia per se on muscle function. Exercise capacity is reduced at altitude, but this may not be due simply to muscle fatigue. In man, during loaded inspiration, the endurance time of the diaphragm is impaired by breathing hypoxic gas mixtures, but it is not clear whether this is due to an action on the central nervous system or a peripheral effect on the respiratory muscles. Thus there are complex interactions between lung disease, hypoxia and respiratory muscle function. Further understanding of these interactions will require improved techniques for identifying and quantifying force generating properties and fatigue of the respiratory muscles.
Several prominent cladists have questioned the importance of fossils in phylogenetic inference, and it is becoming increasingly popular to simply fit extinct forms, if they are considered at all, to a cladogram of Recent data. Gardiner's (1982) and Lovtrup's (1985) study of amniote phylogeny exemplifies this differential treatment, and we focused on that group of organisms to test the proposition that fossils cannot overturn a theory of relationships based only on the Recent biota. Our parsimony analysis of amniote phylogeny, special knowledge contributed by fossils being scrupulously avoided, led to the following best fitting classification, which is similar to the novel hypothesis Gardiner published: (lepidosaurs (turtles (mammals (birds, crocodiles)))). However, adding fossils resulted in a markedly different most parsimonious cladogram of the extant taxa; (mammals (turtles (lepidosaurs (birds, crocodiles)))). The importance of the critical fossils, collectively or individually, seems to reside in their relative primitiveness, and the simplest explanation for their more conservative nature is that they have had less time to evolve. -from Authors
Functional analysis of lung ventilation in salamanders combined with historical analysis of respiratory pumps provides new perspectives on the evolution of breathing mechanisms in vertebrates. Lung ventilation in the aquatic salamander Necturus maculosus was examined by means of cineradiography, measurement of buccal and pleuroperitoneal cavity pressures, and electromyography of hypaxial musculature. In deoxygenated water Necturus periodically rises to the surface, opens its mouth, expands its buccal cavity to draw in fresh air, exhales air from the lungs, closes its mouth, and then compresses its buccal cavity and pumps air into the lungs. Thus Necturus produces only two buccal movements per breath: one expansion and one compression. Necturus shares the use of this two-stroke buccal pump with lungfishes, frogs and other salamanders. The ubiquitous use of this system by basal sarcopterygians is evidence that a two-stroke buccal pump is the primitive lung ventilation mechanism for sarcopterygian vertebrates. In contrast, basal actinopterygian fishes use a four-stroke buccal pump. In these fishes the buccal cavity expands to fill with expired air, compresses to expel the pulmonary air, expands to fill with fresh air, and then compresses for a second time to pump air into the lungs. Whether the sarcopterygian two-stroke buccal pump and the actinopterygian four-stroke buccal pump arose independently, whether both are derived from a single, primitive osteichthyian breathing mechanism, or whether one might be the primitive pattern and the other derived, cannot be determined
Although Necturus and lungfishes both use a two-stroke buccal pump, they differ in their expiration mechanics. Unlike a lungfish (Protopterus), Necturus exhales by contracting a portion of its hypaxial trunk musculature (the m. transversus abdominis) to increase pleuroperitoneal pressure. The occurrence of this same expiratory mechanism in amniotes is evidence that the use of hypaxial musculature for expiration, but not for inspiration, is a primitive tetrapod feature. From this observation we hypothesize that aspiration breathing may have evolved in two stages: initially, from pure buccal pumping to the use of trunk musculature for exhalation but not for inspiration (as in Necturus); and secondarily, to the use of trunk musculature for both exhalation and inhalation by costal aspiration (as in amniotes).
The origin of land vertebrates is a constant subject of discussion. Recent findings in zoology and paleontology (Latimeria, Ichthyostega, Hesperoherpeton, etc.) have supplied many new arguments, but the results arrived at by various authorities show considerable differences. The author is convinced, however, that present knowledge concerning the evolution of tetrapody can be arranged in a harmonious picture. This is the aim of the review. It is concluded that all the evidence speaks in favor of a monophyletic origin of land vertebrates. Among them, the important differences between amphibians on the one side and the reptiles and their descendants on the other are emphasized. The probable sequence with which the various tetrapod features have accumulated, the reasons which prevented the emergence of terrestrial forms from fishes from being ever repeated, and the evolution of the amphibian ontogeny are discussed.
THE traditional classification of reptiles is based on a single key
character, the presence and style of fenestration in the temporal region
of the skull. Snakes, lizards, crocodiles, dinosaurs and others are
'diapsids', in that they have (at least primitively) two holes in the
temporal region. Reptiles in which the skull is completely roofed, with
no temporal fenestration, are the 'anapsids'. These include many
Palaeozoic forms such as captorhinomorphs, procolophonids and
pareiasaurs, but also include Testudines (turtles and tortoises).
Consistent with this assumption, recent analyses of the affinities of
Testudines have included Palaeozoic taxa only, placing them as akin to
captorhinomorphs1 or procolophonids2 or nested
within pareiasaurs3,4. Here we adopt a broader perspective,
adding a range of Mesozoic and extant taxa to the analysis. Our result
robustly supports the diapsid affinities of turtles, and so requires
reassessment of the use of turtles as 'primitive' reptiles in
phylogenetic reconstruction. More generally, it illustrates the
difficulties of treating groups, such as the Testudines, that have
extant members with peculiar morphologies that mask phylogenetic
affinity; the hazards of relying on key characters such as temporal
fenestration, which may mislead; the problems of outgroup choice for
wide-ranging, inclusive analyses that include data from Recent and
extinct groups; and the difficulties of judging the value of parsimony
when applied to such inclusive analyses.
INTRODUCTION Mechanisms for regulating the specific weight of the body are well known in fishes. In other aquatic vertebrates the lungs might have a function similar to that of the swimbladder or the lungs in fishes. In anuran tadpoles the lungs may serve as hydrostatic balancers, but this has not been verified experimentally. Active regulation of lung volume, and thus of body volume and specific weight, during diving is unknown in adult anurans, although Parker (1936) expressed the opinion that in male Trichobatrachus robustus the lungs, which possess a posterior diverticulum surrounded by specialized musculature, serve as a hydrostatic apparatus. If there is no active regulation of lung volume during diving, the volume of the lungs will depend on such factors as pulmonary pressure initially reached while breathing at the surface, compliance of lung wall and body wall, and hydrostatic pressure acting on the body wall. If the volume of the other contents of the body cavity remains unchanged, the lung volume may be expected to adapt by contraction or expansion to the depth at which the animal is located. This expectation is based on the assumption that due to the absence of ribs anurans are unable to expand the body wall except by means of the buccal force pump. If, on the other hand, the musculature of the body wall or of the lungs should act to compress the body cavity or the lungs, pulmonary pressure might be raised to a higher level. This would lead to a decrease in lung volume, an increase in specific weight and facilitation of diving. Relaxation of the muscles would then result in an upward movement of the animal. In this paper the electromyographic activity is described of some muscles
SYNOPSIS. A comparative analysis of actinopterygian and sarcopterygian aerial buccal pumps indicates that the primitive pattern of air transfer differs fundamentally between these two clades. Actinopterygian fishes ventilate their lungs with a four-stroke buccal pump: the buccal cavity expands and fills with expired air, compresses to expel expired air, expands again to take in fresh air, and then compresses again to pump fresh air into the lungs. Lungfishes, caudates, and anurans expand and compress the buccal cavity only once per expiratory-inspiratory cycle, and thus use a two-stroke pump. Both of these bidirectional, aerial buccal pumps evolved from unidirectional, aquatic buccal pumps. The two-stroke aerial pump and the primitive aquatic pump used for gill irrigation share slow movements and may both be triggered by the same central rhythm generator. These similarities suggest that the two-stroke buccal pump evolved from the gill irrigation pump. Similarly, the four-stroke pump shares rapid movement and afferent triggering with aquatic suction feeding and coughing, suggesting that the four-stroke pump may have evolved from a combination of two suction feeding or coughing movements. Thus the differences between the actinopterygian and sarcopterygian aerial buccal pumps may be due to their independent evolution from different aquatic buccal pumps, rather than due to divergence from a single aerial buccal pump.
1.1. Ventilation was measured with pneumotachographs causing pressures <2mm H2O.2.2. Respiratory movements were triphasic (E1-I-E2-pause) but tidal volumes were (a) diphasic because the E2 was against a closed glottis or (b) occasionally triphasic—found in excited (or anaesthetized) lizards in which glottal closure was mistimed (or never occurred) and in most lizards subjected to pressures of > 1 mm Hg from a plethysmograph.3.3. Gular pulsations (contraction-distension-pause) always occurred in sequence with respiration and sometimes in the pause.4.4. Bucco-pharyngeal pumps causing lung ventilation were abnormal.5.5. In 30g L. viridis resting VT = 0.11 ml and f = 30 min−1. Maximum activity caused V́E to increase 24-fold due mainly to VT (12-fold).
Mechanical links between locomotion and respiration are inherently appealing because they may lower the cost of respiration, but they may also limit the ability to adapt ventilation appropriately to physiological needs. Although correlative evidence supports several linkage mechanisms, mechanical links contribute
— Several prominent cladists have questioned the importance of fossils in phylogenctic inference, and it is becoming increasingly popular to simply fit extinct forms, if they are considered at all, to a cladogram of Recent taxa. Gardiner's (1982) and Løvtrup's (1985) study of amniote phylogeny exemplifies this differential treatment, and we focused on that group of organisms to test the proposition that fossils cannot overturn a theory of relationships based only on the Recent biota. Our parsimony analysis of amniote phylogeny, special knowledge contributed by fossils being scrupulously avoided, led to the following best fitting classification, which is similar to the novel hypothesis Gardiner published: (lepidosaurs (turtles (mammals (birds, crocodiles)))). However, adding fossils resulted in a markedly different most parsimonious cladogram of the extant taxa: (mammals (turtles (lepidosaurs (birds, crocodiles)))). That classification is like the traditional hypothesis, and it provides a better fit to the stratigraphic record. To isolate the extinct taxa responsible for the latter classification, the data were successively partitioned with each phylogenetic analysis, and we concluded that: (1) the ingroup, not the outgroup, fossils were important; (2) synapsid, not reptile, fossils were pivotal; (3) certain synapsid fossils, not the earliest or latest, were responsible. The critical nature of the synapsid fossils seemed to lie in the particular combination of primitive and derived character slates they exhibited. Classifying those fossils, along with mammals, as the sister group to the lineage consisting of birds and crocodiles resulted in a relatively poor fit to data; one involving a 2—4 fold increase in evolutionary reversals! Thus, the importance of the critical fossils, collectively or individually, seems to reside in their relative primitive-ness, and the simplest explanation for their more conservative nature is that they have had less time to evolve. While fossils may be important in phylogenetic inference only under certain conditions, there is no compelling reason to prejudge their contribution. We urge systematists to evaluate fairly all of the available evidence.
The respiratory system of insects accomplishes direct gaseous exchange between the tissues and the atmosphere by means of a complicated mechanism. It has been a subject of investigation since the seventeenth century.
The mechanism of lung ventilation in chelonians has been much debated. Electromyographic studies show that the basic mechanism in the snapping turtle, Chelydra serpentina, is dependent on the activities of four major respiratory muscles that are capable of varying the volume of the visceral cavity. The precise mechanism utilized varies in response to environmental factors, especially the depth to which the animal is submerged. Chelydra tends to reduce muscular activity to a minimum, and hydrostatic pressure or gravity replaces muscular effort whenever possible. The response is subject to hysteresis. Both the mechanics and pattern of ventilation in Chelydra differ from those of Testudo. The differences appear to be attributable in part to Chelydra's markedly reduced plastron and more extensive respiratory musculature and in part to the different habitats occupied by the two species.
The mechanism of respiration in the bullfrog has been analyzed by means of pressure recordings from the buccal cavity, the lungs and the abdominal cavity, by cinematography and cinefluorography, and by electromyography of buccal, laryngeal and abdominal muscles. Gas flow was investigated by putting frogs in atmospheres of changing argon and nitrogen content and monitoring the concentration of the nostril efflux.
Three kinds of cyclical phenomena were found. (1) Oscillatory cycles consist of rhythmical raising and lowering of the floor of the mouth, with open nares. They have a definite respiratory function in introducing fresh air into the buccal cavity. (2) Ventilatory cycles involve opening and closing of the glottis and nares and renewal of a portion of the pulmonary gas. More muscles are involved and the pattern of muscular activity is more complex than in the oscillatory cycles. (3) Inflation cycles consist of a series of ventilation cycles, interrupted by an apneic pause. The intensity of the ventilatory cycles increases before this pause and decreases immediately thereafter. This results in a stepwise increase in pulmonary pressure, to a plateau (coincident with the pause) followed by a sudden or stepwise decrease.
The respiratory mechanism depends on the activity of a buccal force pump, which determines pulmonary pressure whose level is always slightly less than the peak pressure values of the ventilation cycles. The elevated pulmonary pressure is responsible for the expulsion of pulmonary gas during the second phase of the next ventilation cycle. This pressure is maintained by the elastic fibers (and the smooth masculature) of the lungs.
The chuckwalla, Sauromalus obesus, avoids predation by wedging itself in a rock crevice and inflating its lungs beyond their normal inspiratory volume. Buccal and pulmonary pressures were recorded in S. obesus during defensive inflation and wedging. Maximum pulmonary pressure generated during defensive wedging was significantly higher and was achieved faster than that of nonwedging inflation. During inflation and wedging, S. obesus forces air into the lungs by pulsatile contraction of the buccal cavity. Buccal pulse pumping is an ancestral ventilation behavior of vertebrates that S. obesus uses for defensive inflation. © Wiley-Liss, Inc.
The pattern of lung ventilation in the terrestrial caecilian Dermophis mexicanus was investigated by recording pressure changes of buccal and pleuroperitoneal cavities and activity of the buccal musculature. This species uses a fairly typical sarcopterygian buccal pumping system to inflate its single lung. What distinguishes it from other amphibians is the large number of buccal pumping cycles that occur in each ventilatory cycle. Up to 29 buccal cycles were observed to occur in a single respiratory cycle, with a mean of 16.1 ± 3.0 buccal cycles. This long series of buccal cycles avoids the sarcopterygian pattern of rebreathing expired air because only the first buccal cycle pumps expired air back into the lung. The series of buccal cycles also generates pleuroperitoneal pressures that are three to ten times greater than those observed in other amphibians. We suggest that these high pleuroperitoneal pressures are necessary for the maintenance of body form and locomotor function in terrestrial caecilians. © 1995 Wiley-Liss, Inc.
In the traditional view of vertebrate lung ventilation mechanisms, air-breathing fishes and amphibians breathe with a buccal pump, and amniotes breathe with an aspiration pump. According to this view, no extant animal exhibits a mechanism that is intermediate between buccal pumping and aspiration breathing; all lung ventilation is produced either by expansion and compression of the mouth cavity via the associated cranial and hyobranchial musculature (buccal pump), or by expansion of the thorax via axial musculature (aspiration pump). However, recent work has shown that amphibians exhibit an intermediate mechanism, in which axial muscles are used for exhalation and a buccal pump is used for inhalation. These findings indicate that aspiration breathing evolved in two steps: first, from pure buccal pumping to the use of axial musculature for exhalation and a buccal pump for inspiration; and second, to full aspiration breathing, in which axial muscles are used for both inhalation and exhalation. Furthermore, the traditional view also holds that buccal pump breathing was lost shortly after aspiration breathing evolved. This view is now being challenged by the discovery that several species of lizards use a buccal pump to augment costal aspiration during exercise. This result, combined with the observation that a behavior known as “buccal oscillation” is found in all amniotes except for mammals, suggests that a reappraisal of the role of buccal pumping in extant and extinct amniotes is in order.
We measured the partitioning of airflow between nasal and oral circuits in five species of lizards before, during and after exercise. Expired gases were measured separately from the mouth and nose circuits in order to estimate the relative contribution of each circuit to ventilatory airflow. Nasal breathing dominates before exercise; however, during exercise the breathing pattern switched to oronasal expiration. Airflow averaged 30% oral expiration across all species during and after exercise. These results have important implications for the design of appropriate masks for respirometry in lizards. In order to ensure that all gases are captured, it is critically important that both the nose and mouth circuits are sampled.
Lungs, rare in fishes today, were apparently very common in early times as an adaptation to then widespread seasonal drought conditions. The development of terrestrial limbs was probably likewise an adaptation promoting aquatic life under such conditions; despite their limbs the earliest amphibians could not become land dwellers because of a dearth of suitable food on land. Skin breathing in modem amphibians is associated with an inefficient type of lung breathing and lack of a developed gill-system to aid in carbon dioxide elimination. But all early amphibians possessed a good rib basket, suggesting a more advanced breathing mechanism, and not improbably many early forms retained functional gills. Further, it is highly probable that all early amphibians were completely scalesheathed. The pedigree of the modern orders is uncertain, but they appear to be specialized forms and not primitive in any regard.
Gular pumping in monitor lizards is known to play an important role in lung ventilation, but its evolutionary origin has not yet been addressed. To determine whether the gular pump derives from the buccal pump of basal tetrapods or is a novel invention, we investigated the electromyographic activity associated with gular pumping in savannah monitor lizards (Varanus exanthematicus). Electrodes were implanted in hyobranchial muscles, and their activity patterns were recorded synchronously with hyoid kinematics, respiratory airflow, and gular pressure. Movement of the highly mobile hyoid apparatus effects large-volume airflows in and out of the gular cavity. The sternohyoideus and branchiohyoideus depress, retract, and abduct the hyoid, thus expanding the gular cavity. The omohyoideus, constrictor colli, intermandibularis, and mandibulohyoideus elevate, protract, and adduct the hyoid, thus compressing the gular cavity. Closure of the choanae by the sublingual plicae precedes gular compression, allowing positive pressure to be generated in the gular cavity to force air into the lungs. The gular pump of monitor lizards is found to exhibit a neuromotor pattern similar to the buccal pump of extant amphibians, and both mechanisms involve homologous muscles. This suggests that the gular pump may have been retained from the ancestral buccal pump. This hypothesis remains to be tested by a broad comparative analysis of gular pumping among the amniotes.
SYNOPSIS. Structural evolution of the vertebrate lung illustrates the principle that the emergence of seemingly new structures such as the mammalian lung is due to intensification of one of the functions of the original piscine lung. The configuration of the mechanical support of the lung in which elastic and collagen fibers form a continuous framework is well matched with the functional demands. The design of the mammalian gas exchange cells is an ingenious solution to meet the functional demands of optimizing maintenance pathways from nucleus to the cytoplasm while simultaneously providing minimal barrier thickness. Surfactant is found in the most primitive lungs providing a protective continuous film of fluid over the delicate epithelium. As the lung became profusely partitioned, surfactant became a functionally new surface-tension reduction device to prevent the collapse of the super-thin foam-like respiratory surface. Experimental analyses have established that in lower vertebrates lungs are ventilated with a buccal pulse pump, which is driven by identical sets of muscles acting in identical patterns in fishes and frogs. In the aquatic habitats suction is the dominant mode of feeding generating buccal pressure changes far exceeding those recorded during air ventilation. From the perspective of air ventilation the buccal pulse pump is overdesigned. However in terrestrial habitats vertebrates must operate with higher metabolic demands and the lung became subdivided into long narrow airways and progressively smaller air spaces, rendering the pulse pump inefficient. With the placement of the lungs inside a pump, the aspiration pump was established. In mammals, the muscular diaphragm represents a key evolutionary innovation since it led to an energetically most efficient aspiration pump. Apparently the potential energy created by contraction of the diaphragm during inhalation is stored in the elastic tissues of the thoracic unit and lung. This energy is released when lung and thorax recoil to bring about exhalation. It is further determined experimentally that respiratory and locomotory patterns are coupled, further maximizing the efficiency of mammalian respiration. Symmorphosis is exhibited in the avian breathing apparatus, which is endowed with a key evolutionary innovation by having the highly specialized lung continuously ventilated by multiple air sacs that function as bellows. Functional morphologists directly deal with these kinds of functional and structural complexities that provide an enormous potential upon simple changes in underlying mechanisms.
Oxygen consumption, body temperature (Tb), and evaporative water loss (mwe) were determined in intact Japanese quail (Coturnix coturnix), and in quail in which the hyoid musculature responsible for gular flutter had been surgically transected several days prior to study. Abolishing gular flutter reduced total mwe by an average of 20% at air temperatures (Ta) above 40 degrees C. Treated birds developed a significantly greater degree of hyperthermia during acute heat stress than the controls and, unlike the controls, were unable to maintain Tb less than Ta above 40 degrees C. These data demonstrate that gular flutter represents a significant cooling mechanism in heat-stressed quail.
The ventilatory mechanics of freely moving Caiman crocodilus were studied by cinefluorescopy and electromyography. The buccal oscillations serve only to flush the internal nares in olfaction. Ventilations are coincident with abdominal oscillations. The larynx ordinarily lies adpressed to the internal nares so that the posterior buccal chamber is excluded from the path of air flow during ventilation and does not contribute to respiratory dead space. The pulmonary pressures may be variably polyphasic and the tracheal flows diphasic. Exhalation involves an anterior shift of the liver by action of the transverse abdominal muscles, while inhalation proceeds due to contraction of the diaphragmatic muscle pulling the liver caudad. The various costal muscles facilitate air flow by shifting the position of the ribs. They also play a role in fixation of the flexible rib cage so that it resists the aspirating and compressing actions of the hepatic piston. The pattern of muscular activity shifts as the trunk is immersed; expiration becomes passive and inspiration requires increased muscular effort. The ribs, instead of changing position with each breath are comparatively fixed by the costal muscles, while changes in the volume of the pleural cavity are caused almost exclusively by movements of the hepatic piston.
We used a high-resolution ultrasound to make electrical recordings from the transversus abdominis muscle in humans. The behavior of this muscle was then compared with that of the external oblique and rectus abdominis in six normal subjects in the seated posture. During voluntary efforts such as expiration from functional residual capacity, speaking, expulsive maneuvers, and isovolume "belly-in" maneuvers, the transversus in general contracted together with the external oblique and the rectus abdominis. In contrast, during hyperoxic hypercapnia, all subjects had phasic expiratory activity in the transversus at ventilations between 10 and 18 l/min, well before activity could be recorded from either the external oblique or the rectus abdominis. Similarly, inspiratory elastic loading evoked transversus expiratory activity in all subjects but external oblique activity in only one subject and rectus abdominis activity in only two subjects. We thus conclude that in humans 1) the transversus abdominis is recruited preferentially to the superficial muscle layer of the abdominal wall during breathing and 2) the threshold for abdominal muscle recruitment during expiration is substantially lower than conventionally thought.
The relative contributions of O2- and CO2-sensitive chemoreceptor information to centrally generated respiratory patterns have changed dramatically during vertebrate evolution. Chemoafferent input from branchial O2 chemoreceptors modulates centrally generated respiratory patterns but is not critical for respiratory rhythmogenesis in fishes. In air-breathing fishes, branchial O2 chemoreceptors monitoring internal and external stimuli control the relative contributions of the gills and air-breathing organ to net ventilation, and chemoafferent input is necessary for initiating air breathing. In the transition from water to air breathing by amphibious vertebrates, rhythmic patterns of branchial ventilation are completely replaced by arrhythmic and intermittent patterns of air breathing, and there is progressive dependence on CO2 as a source of respiratory drive. Periodic initiation of air breathing in resting animals appears to depend on attaining a threshold level of afferent activity from O2- and CO2/pH-sensitive chemoreceptors, since hyperoxia and/or hypocapnia can abolish air breathing in all air-breathing vertebrates. Conversely, chemoreceptor stimulation in amphibians and reptiles converts intermittent to more continuous air breathing patterns, suggesting that adequate biasing input from chemoreceptors activates a central rhythm generator. Chemoafferent input in homeotherms serves as one of several sources of drive for rhythmic breathing and supplies feedback for blood gas homeostasis in the face of metabolic or environmental change.
The central sites of the cardiovascular system (right and left aortic arches, RAo and LAo, pulmonary artery, PA, and right and left atria, RAt and LAt) were chronically and non-occlusively cannulated for an analysis of intracardiac shunting in Varanus niloticus. Oxygen partial pressure (PO2) and oxygen concentration (CO2) were significantly higher in right aortic blood than values determined in left aortic blood. The difference was larger in animals acclimated to 25 degrees C (RAo CO2 = 4.5 +/- 1.00 vol %, LAo CO2 = 3.8 +/- 1.14, X +/- SD, n = 19) than at 35 degrees C (RAo CO2 = 5.8 +/- 1.24, LAo CO2 = 5.4 +/- 1.35, n = 18) (P less than 0.001 for both temperatures, paired t-test). These data are explained by a new model describing the differential shunting patterns of the two aortae in addition to the conventional overall right-to-left and left-to-right shunt fractions. This model was solved on the basis of blood gas data collected by simultaneous multiple-site gas analysis, together with data on the differential blood flow in the central vascular system, collected by application of the microsphere method. At 35 degrees C both right-to-left and left-to-right shunts were relatively small (about 9%), with the right-to-left shunt fraction directed exclusively into the left aorta. Thus right aortic blood represented left atrial blood, whereas left aortic blood was composed of 80% left atrial and 20% right atrial blood. Ninety percent of the pulmonary arterial blood was derived from the right atrium and 10% from the left atrium. At 25 degrees C the composition pattern of effluent blood for each vessel was similar, the absolute flow distribution, however, was different from that at 35 degrees C. These findings are discussed with respect to their significance and compatibility with the wash-out shunt model.