Shell shape does not accurately predict self-righting ability in hatchling freshwater turtles.

Flat hydrodynamic shells likely represent an evolutionary trade-off between adaptation to an aquatic lifestyle and the instability of more rounded shells, thought beneficial for self-righting. Trade-offs often result in compromises, this is particularly true when freshwater turtles, with flatter shells, must self-right to avoid the negative effects of inverting. These turtles, theoretically, invest more biomechanical effort to achieve successful and timely self-righting when compared to turtles with rounded carapaces. This increase in effort places these hatchlings in a precarious position; prone to inversion and predation and with shells seemingly maladapted to the act of self-righting. Here, we examine hatchling self-righting performance in three morphologically distinct freshwater turtle species (Apalone spinifera, Chelydra serpentina and Trachemys scripta scripta) that inhabit similar environmental niches. We demonstrate that these hatchlings were capable of rapid self-righting and used considerably less biomechanical effort relative to adult turtles. Despite differences in shell morphology the energetic efficiency of self-righting remained remarkably low and uniform between the three species. Our results confound theoretical predictions of self-righting ability based on shell shape metrics and indicate that other morphological characteristics like neck or tail morphology and shell material properties must be considered to better understand the biomechanical nuances of Testudine self-righting.

Absence of atrial smooth muscle in the heart of the loggerhead sea turtle (Caretta caretta): a re-evaluation of its role in diving physiology.

Contraction of atrial smooth muscle in the hearts of semi-aquatic emydid turtles regulates ventricular filling, and it has been proposed that it could regulate stroke volume during characteristic rapid transitions in cardiac output associated with diving. For this hypothesis to be supported, atrial smooth muscle should be widely distributed in diving Testudines. To further understand the putative function and evolutionary significance of endocardial smooth muscle in Testudines, we studied the hearts of loggerhead sea turtles, Caretta caretta (n=7), using immunohistochemistry and histology. Surprisingly, we found no evidence of prominent atrial smooth muscle in C. caretta. However, smooth muscle was readily identified in the sinus venosus. Our results suggest that atrial smooth muscle does not contribute to the diving capabilities of C. caretta, indicating that the possible roles of smooth muscle in emydid turtle hearts require a re-evaluation. In sea turtles, the sinus venosus may instead contribute to regulate cardiac filling.

Mediterranean Spur-Thighed Tortoises (Testudo graeca) Have Optimal Speeds at Which They Can Minimise the Metabolic Cost of Transport, on a Treadmill.

Tortoises are famed for their slow locomotion, which is in part related to their herbivorous diet and the constraints imposed by their protective shells. For most animals, the metabolic cost of transport (CoT) is close to the value predicted for their body mass. Testudines appear to be an exception to this rule, as previous studies indicate that, for their body mass, they are economical walkers. The metabolic efficiency of their terrestrial locomotion is explainable by their walking gait biomechanics and the specialisation of their limb muscle physiology, which embodies a predominance of energy-efficient slow-twitch type I muscle fibres. However, there are only two published experimental reports of the energetics of locomotion in tortoises, and these data show high variability. Here, Mediterranean spur-thighed tortoises (Testudo graeca) were trained to walk on a treadmill. Open-flow respirometry and high-speed filming were simultaneously used to measure the metabolic cost of transport and to quantify limb kinematics, respectively. Our data support the low cost of transport previously reported and demonstrate a novel curvilinear relationship to speed in Testudines, suggesting tortoises have an energetically optimal speed range over which they can move in order to minimise the metabolic cost of transport.

The cost of chewing: The energetics and evolutionary significance of mastication in humans.

Any change in the energetic cost of mammalian mastication will affect the net energy gain from foods. Although the energetic efficiency of masticatory effort is fundamental in understanding the evolution of the human masticatory system, nothing is known currently about the associated metabolic costs of chewing different items. Here, using respirometry and electromyography of the masseter muscle, we demonstrate that chewing by human subjects represents a measurable energy sink. Chewing a tasteless odorless gum elevates metabolic rate by 10 to 15% above basal levels. Energy expenditure increases with gum stiffness and is paid for by greater muscle recruitment. For modern humans, it is likely that mastication represents a small part of the daily energy budget. However, for our ancestors, before the onset of cooking and sophisticated food processing methods, the costs must have been relatively high, adding a previously unexplored energetic dimension to the interpretation of hominin dentofacial fossils.

The metabolic cost of turning right side up in the Mediterranean spur-thighed tortoise (Testudo graeca).

Armoured, rigid bodied animals, such as Testudines, must self-right should they find themselves in an inverted position. The ability to self-right is an essential biomechanical and physiological process that influences survival and ultimately fitness. Traits that enhance righting ability may consequently offer an evolutionary advantage. However, the energetic requirements of self-righting are unknown. Using respirometry and kinematic video analysis, we examined the metabolic cost of self-righting in the terrestrial Mediterranean spur-thighed tortoise and compared this to the metabolic cost of locomotion at a moderate, easily sustainable speed. We found that self-righting is, relatively, metabolically expensive and costs around two times the mass-specific power required to walk. Rapid movements of the limbs and head facilitate successful righting however, combined with the constraints of breathing whilst upside down, contribute a significant metabolic cost. Consequently, in the wild, these animals should favour environments or behaviours where the risk of becoming inverted is reduced.

Does posture explain the kinematic differences in a grounded running gait between male and female Svalbard rock ptarmigan (Lagopus muta hyperborea) moving on snow?

The majority of locomotor research is conducted on treadmills and few studies attempt to understand the differences between this and animals moving in the wild. For example, animals may adjust their gait kinematics or limb posture, to a more compliant limb, to increase stability of locomotion to prevent limb failure or falling on different substrates. Here, using video recordings, we compared locomotor parameters (speed range, stride length, stride frequency, stance duration, swing duration and duty factor) of female Svalbard rock ptarmigan (Lagopus muta hyperborea) moving in the wild over snow to previous treadmill-based research. We also compared the absolute and body size (body mass and limb length)-corrected values of kinematic parameters to published data from males to look for any sex differences across walking and grounded running gaits. Our findings indicate that the kinematics of locomotion are largely conserved between the field and laboratory in that none of the female gaits were drastically affected by moving over snow, except for a prolonged swing phase at very slow walking speeds, likely due to toe dragging. Comparisons between the sexes indicate that the differences observed during a walking gait are likely due to body size. However, sexual dimorphism in body size could not explain the disparate grounded running kinematics of the female and male ptarmigan, which might be linked to a more crouched posture in females. Our findings provide insight into how males and females moving in situ may use different strategies to alleviate the effects of a variable substrate. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00300-021-02872-x.

Scaling of axial muscle architecture in juvenile Alligator mississippiensis reveals an enhanced performance capacity of accessory breathing mechanisms.

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.

Turning turtle: scaling relationships and self-righting ability in Chelydra serpentina.

Testudines are susceptible to inversion and self-righting using their necks, limbs or both, to generate enough mechanical force to flip over. We investigated how shell morphology, neck length and self-righting biomechanics scale with body mass during ontogeny in Chelydra serpentina, which uses neck-powered self-righting. We found that younger turtles flipped over twice as fast as older individuals. A simple geometric model predicted the relationships of shell shape and self-righting time with body mass. Conversely, neck force, power output and kinetic energy increase with body mass at rates greater than predicted. These findings were correlated with relatively longer necks in younger turtles than would be predicted by geometric similarity. Therefore, younger turtles self-right with lower biomechanical costs than predicted by simple scaling theory. Considering younger turtles are more prone to inverting and their shells offer less protection, faster and less costly self-righting would be advantageous in overcoming the detriments of inversion.

Examining the accuracy of trackways for predicting gait selection and speed of locomotion.

BACKGROUND: Using Froude numbers (Fr) and relative stride length (stride length: hip height), trackways have been widely used to determine the speed and gait of an animal. This approach, however, is limited by the ability to estimate hip height accurately and by the lack of information related to the substrate properties when the tracks were made, in particular for extinct fauna. By studying the Svalbard ptarmigan moving on snow, we assessed the accuracy of trackway predictions from a species-specific model and two additional Fr based models by ground truthing data extracted from videos as the tracks were being made. RESULTS: The species-specific model accounted for more than 60% of the variability in speed for walking and aerial running, but only accounted for 19% when grounded running, likely due to its stabilizing role while moving faster over a changing substrate. The error in speed estimated was 0-35% for all gaits when using the species-specific model, whereas Fr based estimates produced errors up to 55%. The highest errors were associated with the walking gait. The transition between pendular to bouncing gaits fell close to the estimates using relative stride length described for other extant vertebrates. Conversely, the transition from grounded to aerial running appears to be species specific and highly dependent on posture and substrate. CONCLUSION: Altogether, this study highlights that using trackways to derive predictions on the locomotor speed and gait, using stride length as the only predictor, are problematic as accurate predictions require information from the animal in question.

Inferring cost of transport from whole-body kinematics in three sympatric turtle species with different locomotor habits.

Chelonians are mechanically unusual vertebrates as an exoskeleton limits their body wall mobility. They generally move slowly on land and have aquatic or semi-aquatic lifestyles. Somewhat surprisingly, the limited experimental work that has been done suggests that their energetic cost of transport (CoT) are relatively low. This study examines the mechanical evidence for CoT in three turtle species that have differing degrees of terrestrial activity. Our results show that Apolone travels faster than the other two species, and that Chelydra has higher levels of yaw. All the species show poor mean levels of energy recovery, and, whilst there is considerable variation, never show the high levels of energy recovery seen in cursorial quadrupeds. The mean mechanical CoT is 2 to 4 times higher than is generally seen in terrestrial animals. We therefore find no mechanical support for a low CoT in these species. This study illustrates the need for research on a wider range of chelonians to discover whether there are indeed general trends in mechanical and metabolic energy costs.

Respiratory evolution in archosaurs.

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'.

XROMM kinematics of ventilation in wild turkeys (Meleagris gallopavo).

The avian ribcage is derived relative to other amniotes, and is hypothesised to be constrained in its movements during ventilation. The double-headed ribs form two articulations with the vertebrae, and are thought to rotate about a strict anatomical axis. However, this costovertebral joint constraint has not been demonstrated empirically and was not found in other taxa with double-headed ribs (i.e. crocodilians). Here, we used X-ray reconstruction of moving morphology (XROMM) to quantify rib rotation in wild turkeys (Meleagris gallopavo) during breathing. We demonstrate that, as predicted from anatomy, the ribs do rotate in a hinge-like manner about a single axis. There is also evidence for elliptical motion of the sternum, as has been reported in other taxa. The evolution of the avian ribcage is closely related to the co-evolution of ventilation and flight, and these results are important for how we model ventilation mechanics in living and fossil birds.

Terrestrial locomotion of the Svalbard rock ptarmigan: comparing field and laboratory treadmill studies.

Research into the terrestrial locomotion of birds is often based upon laboratory treadmill experiments. However, it is unclear how transposable these results are for birds moving in the wild. Here, using video recordings, we compared the kinematics of locomotion (stride frequency, stride length, stance phase, swing phase, duty factor) and speed range of Svalbard rock ptarmigan (Lagopus muta hyperborea) under field and laboratory treadmill conditions. Our findings indicate that the kinematics of walking and aerial running are conserved when moving on the treadmill and in the field. Differences, however, were found when grounded running under the two conditions, linked to substrate. Substrate effects were confirmed by analysing trials only moving over very hard snow. In line with laboratory treadmill energetic predictions, wild ptarmigan have a preferred speed during walking and to a lesser extent when aerial running but not when moving with a grounded running gait. The birds were also capable of a higher top speed in the field than that observed during treadmill studies. Our findings demonstrate that laboratory treadmill research provides meaningful information relevant to wild birds while highlighting the importance of understanding the substrate the animals are moving over.

A novel accessory respiratory muscle in the American alligator ( Alligator mississippiensis).

The muscles that effect lung ventilation are key to understanding the evolutionary constraints on animal form and function. Here, through electromyography, we demonstrate a newly discovered respiratory function for the iliocostalis muscle in the American alligator ( Alligator mississippiensis). The iliocostalis is active during expiration when breathing on land at 28°C and this activity is mediated through the uncinate processes on the vertebral ribs. There was also an increase in muscle activity during the forced expirations of alarm distress vocalizations. Interestingly, we did not find any respiratory activity in the iliocostalis when the alligators were breathing with their body submerged in water at 18°C, which resulted in a reduced breathing frequency. The iliocostalis is an accessory breathing muscle that alligators are able to recruit in to assist expiration under certain conditions.

Thermoregulation in rapid growing broiler chickens is compromised by constraints on radiative and convective cooling performance.

Broiler chickens are selected to undergo a rapid six-week hatch-to-slaughter growth phase to attain large body and muscle mass. Broilers have relatively high resting and locomotor metabolic costs suggesting that adaptive thermoregulatory mechanisms are required to dissipate excess heat. Using thermal imaging in the growing broiler we characterised the trajectory of radiative and convective cooling in still air across broiler development. Scaling of head, tarsus and toe surface area did not deviate from body mass2/3 while torso area increased with positive allometry, body mass0.82, reflecting increased feather coverage and/or disproportionate abdominal/thoracic growth. Despite relatively increased area, the body became less effective for heat transfer presumably due to increasing feather coverage. Conversely, the magnitude of heat exchange from the distal hindlimbs was improved in larger birds. Overall capacity to transfer heat by convection and radiation in still air was attenuated over development, since the proportion of resting metabolic rate accounted for decreased in standing and sitting postures. This physiological constraint could be ameliorated by increased latent heat transfer or provision of environmental ventilation, which we modelled according to industrial guidelines. Based on models, higher airspeeds coincided with improved convective cooling that assisted in maintaining the proportion of RMR accounted for by convective and radiative heat transfer. These data highlight the potentially adverse thermoregulatory effects of rapid growth rate and body mass increases, which may contribute to the increased sedentary resting and decreased locomotor behaviour observed in large broilers.

Energy allocation and behaviour in the growing broiler chicken.

Broiler chickens are increasingly at the forefront of global meat production but the consequences of fast growth and selection for an increase in body mass on bird health are an ongoing concern for industry and consumers. To better understand the implications of selection we evaluated energetics and behaviour over the 6-week hatch-to-slaughter developmental period in a commercial broiler. The effect of posture on resting metabolic rate becomes increasingly significant as broilers grow, as standing became more energetically expensive than sitting. The proportion of overall metabolic rate accounted for by locomotor behaviour decreased over development, corresponding to declining activity levels, mean and peak walking speeds. These data are consistent with the inference that broilers allocate energy to activity within a constrained metabolic budget and that there is a reducing metabolic scope for exercise throughout their development. Comparison with similarly sized galliforms reveals that locomotion is relatively energetically expensive in broilers.

Rib kinematics during lung ventilation in the American alligator (Alligator mississippiensis): an XROMM analysis.

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.

The peacock train does not handicap cursorial locomotor performance.

Exaggerated traits, like the peacock train, are recognized as classic examples of sexual selection. The evolution of sexual traits is often considered paradoxical as, although they enhance reproductive success, they are widely presumed to hinder movement and survival. Many exaggerated traits represent an additional mechanical load that must be carried by the animal and therefore may influence the metabolic cost of locomotion and constrain locomotor performance. Here we conducted respirometry experiments on peacocks and demonstrate that the exaggerated sexually selected train does not compromise locomotor performance in terms of the metabolic cost of locomotion and its kinematics. Indeed, peacocks with trains had a lower absolute and mass specific metabolic cost of locomotion. Our findings suggest that adaptations that mitigate any costs associated with exaggerated morphology are central in the evolution of sexually selected traits.

Differential sex-specific walking kinematics in leghorn chickens (Gallus gallus domesticus) selectively bred for different body size.

The differing limb dynamics and postures of small and large terrestrial animals may be mechanisms for minimising metabolic costs under scale-dependent muscle force, work and power demands; however, empirical evidence for this is lacking. Leghorn chickens (Gallus gallus domesticus) are highly dimorphic: males have greater body mass and relative muscle mass than females, which are permanently gravid and have greater relative intestinal mass. Furthermore, leghorns are selected for standard (large) and bantam (small) varieties and the former are sexually dimorphic in posture, with females having a more upright limb. Here, high-speed videography and morphological measurements were used to examine the walking gaits of leghorn chickens of the two varieties and sexes. Hindlimb skeletal elements were geometrically similar among the bird groups, yet the bird groups did not move with dynamic similarity. In agreement with the interspecific scaling of relative duty factor (DF, the proportion of a stride period with ground contact for any given foot) with body mass, bantams walked with greater DF than standards, and females walked with greater DF than males. Greater DF in females than in males was achieved via variety-specific kinematic mechanisms, associated with the presence/absence of postural dimorphism. Females may require greater DF in order to reduce peak muscle forces and minimise power demands associated with lower muscle to reproductive tissue mass ratios and smaller body size. Furthermore, a more upright posture observed in the standard, but not bantam, females, may relate to minimising the work demands of being larger and having proportionally larger reproductive tissue volume. Lower DF in males relative to females may also be a work-minimising strategy and/or due to greater limb inertia (as a result of greater pelvic limb muscle mass) prolonging the swing phase.