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.

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.

Convex hull estimation of mammalian body segment parameters.

Obtaining accurate values for body segment parameters (BSPs) is fundamental in many biomechanical studies, particularly for gait analysis. Convex hulling, where the smallest-possible convex object that surrounds a set of points is calculated, has been suggested as an effective and time-efficient method to estimate these parameters in extinct animals, where soft tissues are rarely preserved. We investigated the effectiveness of convex hull BSP estimation in a range of extant mammals, to inform the potential future usage of this technique with extinct taxa. Computed tomography scans of both the skeleton and skin of every species investigated were virtually segmented. BSPs (the mass, position of the centre of mass and inertial tensors of each segment) were calculated from the resultant soft tissue segments, while the bone segments were used as the basis for convex hull reconstructions. We performed phylogenetic generalized least squares and ordinary least squares regressions to compare the BSPs calculated from soft tissue segments with those estimated using convex hulls, finding consistent predictive relationships for each body segment. The resultant regression equations can, therefore, be used with confidence in future volumetric reconstruction and biomechanical analyses of mammals, in both extinct and extant species where such data may not be available.

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.

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.

Inferring lifestyle for Aves and Theropoda: A model based on curvatures of extant avian ungual bones.

Claws are involved in a number of behaviours including locomotion and prey capture, and as a result animals evolve claw morphologies that enable these functions. Past authors have found geometry of the keratinous sheath of the claw to correlate with mode of life for extant birds and squamates; this relationship has frequently been cited to infer lifestyles for Mesozoic theropods including Archaeopteryx. However, many fossil claws lack keratinous sheaths and thus cannot be analysed using current methods. As the ungual phalanx within the claw is more commonly preserved in the fossil record, geometry of this bone may provide a more useful metric for paleontological analysis. In this study, ungual bones of 108 birds and 5 squamates were imaged using X-ray techniques and a relationship was found between curvatures of the ungual bone within the claw of pedal digit III and four modes of life; ground-dwelling, perching, predatory, and scansorial; using linear discriminant analysis with weighted accuracy equal to 0.79. Our model predicts arboreal lifestyles for Archaeopteryx and Microraptor and a predatory ecology for Confuciusornis. These findings demonstrate the utility of our model in answering questions of palaeoecology, the theropod-bird transition, and the evolution of avian flight. Though the metric exhibits a strong correlation with lifestyle, morphospaces for PD-III curvatures overlap and so this metric should be considered alongside additional evidence.

The biomechanical importance of the scaphoid-centrale fusion during simulated knuckle-walking and its implications for human locomotor evolution.

Inferring the locomotor behaviour of the last common ancestor (LCA) of humans and African apes is still a divisive issue. An African great-ape-like ancestor using knuckle-walking is still the most parsimonious hypothesis for the LCA, despite diverse conflicting lines of evidence. Crucial to this hypothesis is the role of the centrale in the hominoid wrist, since the fusion of this bone with the scaphoid is among the clearest morphological synapomorphies of African apes and hominins. However, the exact functional significance of this fusion remains unclear. We address this question by carrying out finite element simulations of the hominoid wrist during knuckle-walking by virtually generating fused and unfused morphologies in a sample of hominoids. Finite element analysis was applied to test the hypothesis that a fused scaphoid-centrale better withstands the loads derived from knuckle-walking. The results show that fused morphologies display lower stress values, hence supporting a biomechanical explanation for the fusion as a functional adaptation for knuckle-walking. This functional interpretation for the fusion contrasts with the current inferred positional behaviour of the earliest hominins, thus suggesting that this morphology was probably retained from an LCA that exhibited knuckle-walking as part of its locomotor repertoire and that was probably later exapted for other functions.

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.

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.

A Quantitative and Comparative Analysis of the Muscle Architecture of the Forelimb Myology of Diurnal Birds of Prey (Order Accipitriformes and Falconiformes).

Flight is a key feature in the evolution of birds. Wing anatomy reflects many aspects of avian biology such as flight ability. However, our knowledge of the flight musculature has many gaps still, particularly for the distal wing. Therefore, the aim of this work was to investigate the form-function relationship of the forelimb myology of birds to understand the role of individual muscles during flight. Dissections of six species of birds of prey were performed to collect numerical data of muscle architecture, which is the primary determinant of muscle function and force-generation capacity. Birds of prey are a highly diverse group that presents different flight styles throughout the taxa, making them a good model for our purposes. Wing muscle mass (MM) isometrically scaled with body mass1.035 , muscle length to MM0.343 , and fascicle length (FL) scaled allometrically to MM0.285 . The shoulder musculature scaled differently than the other regions where the FL increases more slowly than would be expected in geometrically similar animals, which affects flight mechanics. A proximal-to-distal reduction of MM occurs, which helps to minimize the wing moment of inertia during flight while allowing precise control of the distal wing. Interestingly, the distribution of MM appeared to be species-specific, suggesting a functional signal. This study provides numerical information of muscle architecture of the avian wing that helps us to understand muscle function and its implication in flight, and can be used in future studies of flight mechanics. Anat Rec, 302:1808-1823, 2019. © 2019 American Association for Anatomy.

Pheomelanin pigment remnants mapped in fossils of an extinct mammal.

Recent progress has been made in paleontology with respect to resolving pigmentation in fossil material. Morphological identification of fossilized melanosomes has been one approach, while a second methodology using chemical imaging and spectroscopy has also provided critical information particularly concerning eumelanin (black pigment) residue. In this work we develop the chemical imaging methodology to show that organosulfur-Zn complexes are indicators of pheomelanin (red pigment) in extant and fossil soft tissue and that the mapping of these residual biochemical compounds can be used to restore melanin pigment distribution in a 3 million year old extinct mammal species (Apodemus atavus). Synchotron Rapid Scanning X-ray Fluorescence imaging showed that the distributions of Zn and organic S are correlated within this fossil fur just as in pheomelanin-rich modern integument. Furthermore, Zn coordination chemistry within this fossil fur is closely comparable to that determined from pheomelanin-rich fur and hair standards. The non-destructive methods presented here provide a protocol for detecting residual pheomelanin in precious specimens.

Vertebral morphometrics and lung structure in non-avian dinosaurs.

The lung-air sac system of modern birds is unique among vertebrates. However, debate surrounds whether an avian-style lung is restricted to birds or first appeared in their dinosaurian ancestors, as common osteological correlates for the respiratory system offer limited information on the lungs themselves. Here, we shed light on these issues by using axial morphology as a direct osteological correlate of lung structure, and quantifying vertebral shape using geometric morphometrics in birds, crocodilians and a wide range of dinosaurian taxa. Although fully avian lungs were a rather late innovation, we quantitatively show that non-avian dinosaurs and basal dinosauriforms possessed bird-like costovertebral joints and a furrowed thoracic ceiling. This would have immobilized the lung's dorsal surface, a structural prerequisite for a thinned blood-gas barrier and increased gas exchange potential. This could have permitted high levels of aerobic and metabolic activity in dinosaurs, even in the hypoxic conditions of the Mesozoic, contributing to their successful radiation.

Inferring locomotor behaviours in Miocene New World monkeys using finite element analysis, geometric morphometrics and machine-learning classification techniques applied to talar morphology.

The talus is one of the most commonly preserved post-cranial elements in the platyrrhine fossil record. Talar morphology can provide information about postural adaptations because it is the anatomical structure responsible for transmitting body mass forces from the leg to the foot. The aim of this study is to test whether the locomotor behaviour of fossil Miocene platyrrhines could be inferred from their talus morphology. The extant sample was classified into three different locomotor categories and then talar strength was compared using finite-element analysis. Geometric morphometrics were used to quantify talar shape and to assess its association with biomechanical strength. Finally, several machine-learning (ML) algorithms were trained using both the biomechanical and morphometric data from the extant taxa to infer the possible locomotor behaviour of the Miocene fossil sample. The obtained results show that the different locomotor categories are distinguishable using either biomechanical or morphometric data. The ML algorithms categorized most of the fossil sample as arboreal quadrupeds. This study has shown that a combined approach can contribute to the understanding of platyrrhine talar morphology and its relationship with locomotion. This approach is likely to be beneficial for determining the locomotor habits in other fossil taxa.

Energy and time optimal trajectories in exploratory jumps of the spider Phidippus regius.

Jumping spiders are proficient jumpers that use jumps in a variety of behavioural contexts. We use high speed, high resolution video to measure the kinematics of a single regal jumping spider for a total of 15 different tasks based on a horizontal gap of 2-5 body lengths and vertical gap of +/-2 body lengths. For short range jumps, we show that low angled trajectories are used that minimise flight time. For longer jumps, take-off angles are steeper and closer to the optimum for minimum energy cost of transport. Comparison of jump performance against other arthropods shows that Phidippus regius is firmly in the group of animals that use dynamic muscle contraction for actuation as opposed to a stored energy catapult system. We find that the jump power requirements can be met from the estimated mass of leg muscle; hydraulic augmentation may be present but appears not to be energetically essential.

Analyzing the sclerocarpy adaptations of the Pitheciidae mandible.

Primates are interpreted to be ancestrally adapted to frugivory, although some modern groups show clear adaptations to other diets. Among them, pitheciids stand out for specifically predating seeds. This dietary specialization is known as sclerocarpy and refers to the extraction of seeds from surrounding hard tissues using the anterior dentition followed by the mastication of seeds by the molars. It has been proposed that Callicebus-Pithecia-Chiropotes-Cacajao represent a morphocline of increasingly specialized anatomical traits for sclerocarpic foraging. This study addresses whether there is a sclerocarpic specialization gradient in the mandibular morphology of pitheciids. Finite element analysis (FEA) was used to simulate two biting scenarios and the obtained stress values were compared between different pitheciids. Geometric morphometrics (GM) were used to display the morphological variation of this group. No support was found for the morphocline hypothesis from a biomechanical viewpoint since all pitheciins showed similar stress values and on average Chiropotes rather than Cacajao exhibited the strongest mandible. From a morphological perspective, it was found that there is indeed relative "robusticity" continuum in the pitheciid mandible for some aspects of shape as expected for the morphocline hypothesis, but this gradient could be related to other factors rather than sclerocarpic specialization. The present results are expected to contribute to a better insight regarding the ecomorphological relationship between mandibular morphology and mechanical performance among pitheciids.

A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds.

Fossils of juvenile Mesozoic birds provide insight into the early evolution of avian development, however such fossils are rare. The analysis of the ossification sequence in these early-branching birds has the potential to address important questions about their comparative developmental biology and to help understand their morphological evolution and ecological differentiation. Here we report on an early juvenile enantiornithine specimen from the Early Cretaceous of Europe, which sheds new light on the osteogenesis in this most species-rich clade of Mesozoic birds. Consisting of a nearly complete skeleton, it is amongst the smallest known Mesozoic avian fossils representing post-hatching stages of development. Comparisons between this new specimen and other known early juvenile enantiornithines support a clade-wide asynchronous pattern of osteogenesis in the sternum and the vertebral column, and strongly indicate that the hatchlings of these phylogenetically basal birds varied greatly in size and tempo of skeletal maturation.

A volumetric technique for fossil body mass estimation applied to Australopithecus afarensis.

Fossil body mass estimation is a well established practice within the field of physical anthropology. Previous studies have relied upon traditional allometric approaches, in which the relationship between one/several skeletal dimensions and body mass in a range of modern taxa is used in a predictive capacity. The lack of relatively complete skeletons has thus far limited the potential application of alternative mass estimation techniques, such as volumetric reconstruction, to fossil hominins. Yet across vertebrate paleontology more broadly, novel volumetric approaches are resulting in predicted values for fossil body mass very different to those estimated by traditional allometry. Here we present a new digital reconstruction of Australopithecus afarensis (A.L. 288-1; 'Lucy') and a convex hull-based volumetric estimate of body mass. The technique relies upon identifying a predictable relationship between the 'shrink-wrapped' volume of the skeleton and known body mass in a range of modern taxa, and subsequent application to an articulated model of the fossil taxa of interest. Our calibration dataset comprises whole body computed tomography (CT) scans of 15 species of modern primate. The resulting predictive model is characterized by a high correlation coefficient (r2 = 0.988) and a percentage standard error of 20%, and performs well when applied to modern individuals of known body mass. Application of the convex hull technique to A. afarensis results in a relatively low body mass estimate of 20.4 kg (95% prediction interval 13.5-30.9 kg). A sensitivity analysis on the articulation of the chest region highlights the sensitivity of our approach to the reconstruction of the trunk, and the incomplete nature of the preserved ribcage may explain the low values for predicted body mass here. We suggest that the heaviest of previous estimates would require the thorax to be expanded to an unlikely extent, yet this can only be properly tested when more complete fossils are available.