Reverse-engineering the locomotion of a stem amniote.

Reconstructing the locomotion of extinct vertebrates offers insights into their palaeobiology and helps to conceptualize major transitions in vertebrate evolution1-4. However, estimating the locomotor behaviour of a fossil species remains a challenge because of the limited information preserved and the lack of a direct correspondence between form and function5,6. The evolution of advanced locomotion on land-that is, locomotion that is more erect, balanced and mechanically power-saving than is assumed of anamniote early tetrapods-has previously been linked to the terrestrialization and diversification of amniote lineages7. To our knowledge, no reconstructions of the locomotor characteristics of stem amniotes based on multiple quantitative methods have previously been attempted: previous methods have relied on anatomical features alone, ambiguous locomotor information preserved in ichnofossils or unspecific modelling of locomotor dynamics. Here we quantitatively examine plausible gaits of the stem amniote Orobates pabsti, a species that is known from a complete body fossil preserved in association with trackways8. We reconstruct likely gaits that match the footprints, and investigate whether Orobates exhibited locomotor characteristics that have previously been linked to the diversification of crown amniotes. Our integrative methodology uses constraints derived from biomechanically relevant metrics, which also apply to extant tetrapods. The framework uses in vivo assessment of locomotor mechanics in four extant species to guide an anatomically informed kinematic simulation of Orobates, as well as dynamic simulations and robotics to filter the parameter space for plausible gaits. The approach was validated using two extant species that have different morphologies, gaits and footprints. Our metrics indicate that Orobates exhibited more advanced locomotion than has previously been assumed for earlier tetrapods7,9, which suggests that advanced terrestrial locomotion preceded the diversification of crown amniotes. We provide an accompanying website for the exploration of the filters that constrain our simulations, which will allow revision of our approach using new data, assumptions or methods.

The functional significance of aberrant cervical counts in sloths: insights from automated exhaustive analysis of cervical range of motion.

Besides manatees, the suspensory extant 'tree sloths' are the only mammals that deviate from a cervical count (CC) of seven vertebrae. They do so in opposite directions in the two living genera (increased versus decreased CC). Aberrant CCs seemingly reflect neck mobility in both genera, suggesting adaptive significance for their head position during suspensory locomotion and especially increased ability for neck torsion in three-toed sloths. We test two hypotheses in a comparative evolutionary framework by assessing three-dimensional intervertebral range of motion (ROM) based on exhaustive automated detection of bone collisions and joint disarticulation while accounting for interacting rotations of roll, yaw and pitch. First, we hypothesize that the increase of CC also increases overall neck mobility compared with mammals with a regular CC, and vice versa. Second, we hypothesize that the anatomy of the intervertebral articulations determines mobility of the neck. The assessment revealed that CC plays only a secondary role in defining ROM since summed torsion (roll) capacity was primarily determined by vertebral anatomy. Our results thus suggest limited neck rotational adaptive significance of the CC aberration in sloths. Further, the study demonstrates the suitability of our automated approach for the comparative assessment of osteological ROM in vertebral series.

Ontogeny of a tessellated surface: Carapace growth of the longhorn cowfish Lactoria cornuta.

Biological armors derive their mechanical integrity in part from their geometric architectures, often involving tessellations: individual structural elements tiled together to form surface shells. The carapace of boxfish, for example, is composed of mineralized polygonal plates, called scutes, arranged in a complex geometric pattern and nearly completely encasing the body. In contrast to artificial armors, the boxfish exoskeleton grows with the fish; the relationship between the tessellation and the gross structure of the armor is therefore critical to sustained protection throughout growth. To clarify whether or how the boxfish tessellation is maintained or altered with age, we quantify architectural aspects of the tessellated carapace of the longhorn cowfish Lactoria cornuta through ontogeny (across nearly an order of magnitude in standard length) and in a high-throughput fashion, using high-resolution microCT data and segmentation algorithms to characterize the hundreds of scutes that cover each individual. We show that carapace growth is canalized with little variability across individuals: rather than continually adding scutes to enlarge the carapace surface, the number of scutes is surprisingly constant, with scutes increasing in volume, thickness, and especially width with age. As cowfish and their scutes grow, scutes become comparatively thinner, with the scutes at the edges (weak points in a boxy architecture) being some of the thickest and most reinforced in younger animals and thinning most slowly across ontogeny. In contrast, smaller scutes with more variable curvature were found in the limited areas of more complex topology (e.g., around fin insertions, mouth, and anus). Measurements of Gaussian and mean curvature illustrate that cowfish are essentially tessellated boxes throughout life: predominantly zero curvature surfaces comprised of mostly flat scutes, and with scutes with sharp bends used sparingly to form box edges. Since growth of a curved, tiled surface with a fixed number of tiles would require tile restructuring to accommodate the surface's changing radius of curvature, our results therefore illustrate a previously unappreciated advantage of the odd boxfish morphology: by having predominantly flat surfaces, it is the box-like body form that in fact permits a relatively straightforward growth system of this tessellated architecture (i.e., where material is added to scute edges). Our characterization of the ontogeny and maintenance of the carapace tessellation provides insights into the potentially conflicting mechanical, geometric, and developmental constraints of this species but also perspectives into natural strategies for constructing mutable tiled architectures.

A therian mammal with sprawling kinematics? Gait and 3D forelimb X-ray motion analysis in tamanduas.

Therian mammals are known to move their forelimbs in a parasagittal plane, retracting the mobilised scapula during stance phase. Non-cursorial therian mammals often abduct the elbow out of the shoulder-hip parasagittal plane. This is especially prominent in Tamandua (Xenarthra), which suggests they employ aspects of sprawling (e.g. lizard-like) locomotion. Here, we tested whether tamanduas use sprawling forelimb kinematics, i.e. a largely immobile scapula with pronounced lateral spine bending and long-axis rotation of the humerus. We analysed high-speed videos and used X-ray motion analysis of tamanduas walking and balancing on branches of varying inclinations and provide a quantitative characterization of gaits and forelimb kinematics. Tamanduas displayed lateral sequence/lateral couplets on flat ground and horizontal branches, but increased diagonality on steeper inclines and declines, resulting in lateral sequence/diagonal couplets gaits. This result provides further evidence for high diagonality in arboreal species, probably maximising stability in arboreal environments. Further, the results reveal a mosaic of sprawling and parasagittal kinematic characteristics. The abducted elbow results from a constantly internally rotated scapula about its long axis and a retracted humerus. Scapula retraction contributes considerably to stride length. However, lateral rotation in the pectoral region of the spine (range: 21 deg) is higher than reported for other therian mammals. Instead, it is similar to that of skinks and alligators, indicating an aspect generally associated with sprawling locomotion is characteristic for forelimb kinematics of tamanduas. Our study contributes to a growing body of evidence of highly variable non-cursorial therian mammal locomotor kinematics.

Variation in limb loading magnitude and timing in tetrapods.

Comparative analyses of locomotion in tetrapods reveal two patterns of stride cycle variability. Tachymetabolic tetrapods (birds and mammals) have lower inter-cycle variation in stride duration than bradymetabolic tetrapods (amphibians, lizards, turtles and crocodilians). This pattern has been linked to the fact that birds and mammals share enlarged cerebella, relatively enlarged and heavily myelinated Ia afferents, and γ-motoneurons to their muscle spindles. Both tachymetabolic tetrapod lineages also possess an encapsulated Golgi tendon morphology, thought to provide more spatially precise information on muscle tension. The functional consequence of this derived Golgi tendon morphology has never been tested. We hypothesized that one advantage of precise information on muscle tension would be lower and more predictable limb bone stresses, achieved in tachymetabolic tetrapods by having less variable substrate reaction forces than bradymetabolic tetrapods. To test this hypothesis, we analyzed hindlimb substrate reaction forces during locomotion of 55 tetrapod species in a phylogenetic comparative framework. Variation in species means of limb loading magnitude and timing confirm that, for most of the variables analyzed, variance in hindlimb loading and timing is significantly lower in species with encapsulated versus unencapsulated Golgi tendon organs. These findings suggest that maintaining predictable limb loading provides a selective advantage for birds and mammals by allowing energy savings during locomotion, lower limb bone safety factors and quicker recovery from perturbations. The importance of variation in other biomechanical variables in explaining these patterns, such as posture, effective mechanical advantage and center-of-mass mechanics, remains to be clarified.

Femoral morphology of sciuromorph rodents in light of scaling and locomotor ecology.

Sciuromorph rodents are a monophyletic group comprising about 300 species with a body mass range spanning three orders of magnitude and various locomotor behaviors that we categorized into arboreal, fossorial and aerial. The purpose of this study was to investigate how the interplay of locomotor ecology and body mass affects the morphology of the sciuromorph locomotor apparatus. The most proximal skeletal element of the hind limb, i.e. the femur, was selected, because it was shown to reflect a functional signal in various mammalian taxa. We analyzed univariate traits (effective femoral length, various robustness variables and the in-levers of the muscles attaching to the greater, third and lesser trochanters) as well as femoral shape, representing a multivariate trait. An ordinary least-squares regression including 177 species was used to test for a significant interaction effect between body mass and locomotor ecology on the variables. Specifically, it tested whether the scaling patterns of the fossorial and aerial groups differ when compared with the arboreal, because the latter was identified as the ancestral sciuromorph condition via stochastic character mapping. We expected aerial species to display the highest trait values for a given body mass as well as the steepest slopes, followed by the arboreal and fossorial species along this order. An Ornstein-Uhlenbeck regression fitted to a phylogenetically pruned dataset of 140 species revealed the phylogenetic inertia to be very low in the univariate traits, hence justifying the utilization of standard regressions. These variables generally scaled close to isometry, suggesting that scaling adjustments might not have played a major role for most of the femoral features. Nevertheless, the low phylogenetic inertia indicates that the observed scaling patterns needed to be maintained during sciuromorph evolution. Significant interaction effects were discovered in the femoral length, the centroid size of the condyles, and the in-levers of the greater and third trochanters. Additionally, adjustments in various femoral traits reflect the acquisitions of fossorial and aerial behaviors from arboreal ancestors. Using sciuromorphs as a focal clade, our findings exemplify the importance of statistically accounting for potential interaction effects of different environmental factors in studies relating morphology to ecology.

Homeotic transformations reflect departure from the mammalian 'rule of seven' cervical vertebrae in sloths: inferences on the Hox code and morphological modularity of the mammalian neck.

BACKGROUND: Sloths are one of only two exceptions to the mammalian 'rule of seven' vertebrae in the neck. As a striking case of breaking the evolutionary constraint, the explanation for the exceptional number of cervical vertebrae in sloths is still under debate. Two diverging hypotheses, both ultimately linked to the low metabolic rate of sloths, have been proposed: hypothesis 1 involves morphological transformation of vertebrae due to changes in the Hox gene expression pattern and hypothesis 2 assumes that the Hox gene expression pattern is not altered and the identity of the vertebrae is not changed. Direct evidence supporting either hypothesis would involve knowledge of the vertebral Hox code in sloths, but the realization of such studies is extremely limited. Here, on the basis of the previously established correlation between anterior Hox gene expression and the quantifiable vertebral shape, we present the morphological regionalization of the neck in three different species of sloths with aberrant cervical count providing indirect insight into the vertebral Hox code. RESULTS: Shape differences within the cervical vertebral column suggest a mouse-like Hox code in the neck of sloths. We infer an anterior shift of HoxC-6 expression in association with the first thoracic vertebra in short-necked sloths with decreased cervical count, and a posterior shift of HoxC-5 and HoxC-6 expression in long-necked sloths with increased cervical count. CONCLUSION: Although only future developmental analyses in non-model organisms, such as sloths, will yield direct evidence for the evolutionary mechanism responsible for the aberrant number of cervical vertebrae, our observations lend support to hypothesis 1 indicating that the number of modules is retained but their boundaries are displaced. Our approach based on quantified morphological differences also provides a reliable basis for further research including fossil taxa such as extinct 'ground sloths' in order to trace the pattern and the underlying genetic mechanisms in the evolution of the vertebral column in mammals.

Bone cortical compactness in 'tree sloths' reflects convergent evolution.

Bone remodeling, one of the main processes that regulate bone microstructure, consists of bone resorption followed by the deposition of secondary bone at the same location. Remodeling intensity varies among taxa, but a characteristically compact cortex is ubiquitous in the long bones of mature terrestrial mammals. A previous analysis found that cortical bone in a few 'tree sloth' (Bradypus and Choloepus) specimens is heavily remodeled and characterized by numerous immature secondary osteons, suggesting that these animals were remodeling their bones at high rate until late in their ontogeny. This study aims at testing if this remodeling is generally present in 'tree sloths', using a quantitative analysis of the humeral cortical compactness (CC) among xenarthrans. The results of the investigation of humeral diaphyseal cross-sections of 26 specimens belonging to 10 xenarthran species including specimens from both extinct and extant species indicate that in 'tree sloths' the CC is significantly lower than in the other sampled xenarthrans. No significant difference was found between the CC of the two genera of 'tree sloths'. Our results are consistent with the hypothesis that the cortical bone of 'tree sloths' in general undergoes intense and balanced remodeling that is maintained until late (possibly throughout) in their ontogeny. In the light of xenarthran phylogeny, low CC represents another convergence between the long-separated 'tree sloth' lineages. Although the exact structural and/or functional demands that are associated with this trait are hitherto unknown, several hypotheses are suggested here, including a relationship to their relatively low metabolism and to the mechanical demands imposed upon the bones by the suspensory posture and locomotion, which was independently acquired by the two genera of 'tree sloths'.

Barn owls maximize head rotations by a combination of yawing and rolling in functionally diverse regions of the neck.

Owls are known for their outstanding neck mobility: these birds can rotate their heads more than 270°. The anatomical basis of this extraordinary neck rotation ability is not well understood. We used X-ray fluoroscopy of living owls as well as forced neck rotations in dead specimens and computer tomographic (CT) reconstructions to study how the individual cervical joints contribute to head rotation in barn owls (Tyto furcata pratincola). The X-ray data showed the natural posture of the neck, and the reconstructions of the CT-scans provided the shapes of the individual vertebrae. Joint mobility was analyzed in a spherical coordinate system. The rotational capability was described as rotation about the yaw and roll axes. The analyses suggest a functional division of the cervical spine into several regions. Most importantly, an upper region shows high rolling and yawing capabilities. The mobility of the lower, more horizontally oriented joints of the cervical spine is restricted mainly to the roll axis. These rolling movements lead to lateral bending, effectively resulting in a side shift of the head compared with the trunk during large rotations. The joints in the middle of the cervical spine proved to contribute less to head rotation. The analysis of joint mobility demonstrated how owls might maximize horizontal head rotation by a specific and variable combination of yawing and rolling in functionally diverse regions of the neck.

Trabecular architecture in the forelimb epiphyses of extant xenarthrans (Mammalia).

BACKGROUND: Bone structure has a crucial role in the functional adaptations that allow vertebrates to conduct their diverse lifestyles. Much has been documented regarding the diaphyseal structure of long bones of tetrapods. However, the architecture of trabecular bone, which is for instance found within the epiphyses of long bones, and which has been shown experimentally to be extremely plastic, has received little attention in the context of lifestyle adaptations (virtually only in primates). We therefore investigated the forelimb epiphyses of extant xenarthrans, the placental mammals including the sloths, anteaters, and armadillos. They are characterised by several lifestyles and degrees of fossoriality involving distinct uses of their forelimb. We used micro computed tomography data to acquire 3D trabecular parameters at regions of interest (ROIs) for all extant genera of xenarthrans (with replicates). Traditional, spherical, and phylogenetically informed statistics (including the consideration of size effects) were used to characterise the functional signal of these parameters. RESULTS: Several trabecular parameters yielded functional distinctions. The main direction of the trabeculae distinguished lifestyle categories for one ROI (the radial trochlea). Among the other trabecular parameters, it is the degree of anisotropy (i.e., a preferential alignment of the trabeculae) that yielded the clearest functional signal. For all ROIs, the armadillos, which represent the fully terrestrial and fossorial category, were found as characterised by a greater degree of anisotropy (i.e., more aligned trabeculae). Furthermore, the trabeculae of the humeral head of the most fossorial armadillos were also found to be more anisotropic than in the less fossorial species. CONCLUSIONS: Most parameters were marked by an important intraspecific variability and by a size effect, which could, at least partly, be masking the functional signal. But for some parameters, the degree of anisotropy in particular, a clear functional distinction was recovered. Along with data on primates, our findings suggest that a trabecular architecture characterised by a greater degree of anisotropy is to be expected in species in which the relevant epiphyses withstand a restricted range of load directions. Trabecular architecture therefore is a promising research avenue for the reconstruction of lifestyles in extinct or cryptic species.

Timing of head movements is consistent with energy minimization in walking ungulates.

Many ungulates show a conspicuous nodding motion of the head when walking. Until now, the functional significance of this behaviour remained unclear. Combining in vivo kinematics of quadrupedal mammals with a computer model, we show that the timing of vertical displacements of the head and neck is consistent with minimizing energy expenditure for carrying these body parts in an inverted pendulum walking gait. Varying the timing of head movements in the model resulted in increased metabolic cost estimate for carrying the head and neck of up to 63%. Oscillations of the head-neck unit result in weight force oscillations transmitted to the forelimbs. Advantageous timing increases the load in single support phases, in which redirecting the trajectory of the centre of mass (COM) is thought to be energetically inexpensive. During double support, in which-according to collision mechanics-directional changes of the impulse of the COM are expensive, the observed timing decreases the load. Because the head and neck comprise approximately 10% of body mass, the effect shown here should also affect the animals' overall energy expenditure. This mechanism, working analogously in high-tech backpacks for energy-saving load carriage, is widespread in ungulates, and provides insight into how animals economize locomotion.

Morphology and motion: hindlimb proportions and swing phase kinematics in terrestrially locomoting charadriiform birds.

Differing limb proportions in terms of length and mass, as well as differences in mass being concentrated proximally or distally, influence the limb's moment of inertia (MOI), which represents its resistance to being swung. Limb morphology - including limb segment proportions - thus probably has direct relevance for the metabolic cost of swinging the limb during locomotion. However, it remains largely unexplored how differences in limb proportions influence limb kinematics during swing phase. To test whether differences in limb proportions are associated with differences in swing phase kinematics, we collected hindlimb kinematic data from three species of charadriiform birds differing widely in their hindlimb proportions: lapwings, oystercatchers and avocets. Using these three species, we tested for differences in maximum joint flexion, maximum joint extension and range of motion (RoM), in addition to differences in maximum segment angular velocity and excursion. We found that the taxa with greater limb MOI - oystercatchers and avocets - flex their limbs more than lapwings. However, we found no consistent differences in joint extension and RoM among species. Likewise, we found no consistent differences in limb segment angular velocity and excursion, indicating that differences in limb inertia in these three avian species do not necessarily underlie the rate or extent of limb segment movements. The observed increased limb flexion among these taxa with distally heavy limbs resulted in reduced MOI of the limb when compared with a neutral pose. A trade-off between exerting force to actively flex the limb and potential savings by a reduction of MOI is skewed towards reducing the limb's MOI as a result of MOI being in part a function of the radius of gyration squared. Increased limb flexion is a likely means to lower the cost of swinging the limbs.

Trunk orientation causes asymmetries in leg function in small bird terrestrial locomotion.

In contrast to the upright trunk in humans, trunk orientation in most birds is almost horizontal (pronograde). It is conceivable that the orientation of the heavy trunk strongly influences the dynamics of bipedal terrestrial locomotion. Here, we analyse for the first time the effects of a pronograde trunk orientation on leg function and stability during bipedal locomotion. For this, we first inferred the leg function and trunk control strategy applied by a generalized small bird during terrestrial locomotion by analysing synchronously recorded kinematic (three-dimensional X-ray videography) and kinetic (three-dimensional force measurement) quail locomotion data. Then, by simulating quail gaits using a simplistic bioinspired numerical model which made use of parameters obtained in in vivo experiments with real quail, we show that the observed asymmetric leg function (left-skewed ground reaction force and longer leg at touchdown than at lift-off) is necessary for pronograde steady-state locomotion. In addition, steady-state locomotion becomes stable for specific morphological parameters. For quail-like parameters, the most common stable solution is grounded running, a gait preferred by quail and most of the other small birds. We hypothesize that stability of bipedal locomotion is a functional demand that, depending on trunk orientation and centre of mass location, constrains basic hind limb morphology and function, such as leg length, leg stiffness and leg damping.

Soft tissue influence on ex vivo mobility in the hip of Iguana: comparison with in vivo movement and its bearing on joint motion of fossil sprawling tetrapods.

The reconstruction of a joint's maximum range of mobility (ROM) often is a first step when trying to understand the locomotion of fossil tetrapods. But previous studies suggest that the ROM of a joint is restricted by soft tissues surrounding the joint. To expand the limited informative value of ROM studies for the reconstruction of a fossil species' locomotor characteristics, it is moreover necessary to better understand the relationship of ex vivo ROM with the actual in vivo joint movement. To gain insight into the relationship between ex vivo mobility and in vivo movement, we systematically tested for the influence of soft tissues on joint ROM in the hip of the modern lizard Iguana iguana. Then, we compared the ex vivo mobility to in vivo kinematics of the hip joint in the same specimens using X-ray sequences of steady-state treadmill locomotion previously recorded. With stepwise removal of soft tissues and a repeated-measurement protocol, we show that soft tissues surrounding the hip joint considerably limit ROM, highlighting the problems when joint ROM is deduced from bare bones only. We found the integument to have the largest effect on the range of long-axis rotation, pro- and retraction. Importantly, during locomotion the iguana used only a fragment of the ROM that was measured in our least restrictive dissection situation (i.e. pelvis and femur only conjoined by ligaments), demonstrating the discrepancy between hip joint ROM and actual in vivo movement. Our study emphasizes the necessity for caution when attempting to reconstruct joint ROM or even locomotor kinematics from fossil bones only, as actual in vivo movement cannot be deduced directly from any condition of cadaver mobility in Iguana and likely in other tetrapods.

On vision in birds: coordination of head-bobbing and gait stabilises vertical head position in quail.

INTRODUCTION: Head-bobbing in birds is a conspicuous behaviour related to vision comprising a hold phase and a thrust phase. The timing of these phases has been shown in many birds, including quail, to be coordinated with footfall during locomotion. We were interested in the biomechanics behind this phenomenon. During terrestrial locomotion in birds, the trunk is subjected to gait-specific vertical oscillations. Without compensation, these vertical oscillations conflict with the demands of vision (i.e., a vertically stable head position). We tested the hypothesis that the coordination between head-bobbing and trunk movement is a means of reconciling the conflicting demands of vision and locomotion which should thus vary according to gait. RESULTS: Significant differences in the timing of head-bobbing were found between gaits. The thrust phase was initiated just prior to the double support phase in walking (vaulting) trials, whereas in running (bouncing) trials, thrust started around midstance. Altering the timing of head-trunk-coordination in simulations showed that the timing naturally favoured by birds minimizes the vertical displacement of the head. When using a bouncing gait the timing of head bobbing had a compensatory effect on the fluctuation of the potential energy of the bird's centre of mass. CONCLUSION: The results are consistent with expectations based on the vertical trunk fluctuations observed in biomechanical models of vaulting and bouncing locomotion. The timing of the head-bobbing behaviour naturally favoured by quail benefits vision during vaulting and bouncing gaits and potentially helps reducing the mechanical cost associated with head bobbing when using a bouncing gait.

Planar covariation of limb elevation angles during bipedal locomotion in common quails (Coturnix coturnix).

In human bipedal walking, temporal changes in the elevation angle of the thigh, shank and foot segments covary to form a regular loop within a single plane in three-dimensional space. In this study, we quantified the planar covariation of limb elevation angles during bipedal locomotion in common quails to test whether the degree of planarity and the orientation of the covariance plane differ between birds, humans and Japanese macaques as reported in published accounts. Five quails locomoted on a treadmill and were recorded by a lateral X-ray fluoroscopy. The elevation angle of the thigh, shank and foot segments relative to the vertical axis was calculated and compared with published data on human and macaque bipedal locomotion. The results showed that the planar covariation applied to quail bipedal locomotion and planarity was stronger in quails than in humans. The orientation of the covariation plane in quails differed from that in humans, and was more similar to the orientation of the covariation plane in macaques. Although human walking is characterized by vaulting mechanics of the body center of mass, quails and macaques utilize spring-like running mechanics even though the duty factor is >0.5. Therefore, differences in the stance leg mechanics between quails and humans may underlie the difference in the orientation of the covariation plane. The planar covariation of inter-segmental coordination has evolved independently in both avian and human locomotion, despite the different mechanical constraints.

Comparative finite element analysis of the first thoracic vertebra in artiodactyls.

Artiodactyls exhibit a striking diversity of the cervical vertebral column in terms of length and overall mobility. Using finite element analysis, this study explores the morphology at the cervico-thoracic boundary and its performance under loads in artiodactyls with different habitual neck postures and body sizes. The first thoracic vertebra of 36 species was loaded with (i) a compressive load on the vertebral body to model the weight of the head and neck exerted onto the trunk; and (ii) a tensile load at the spinous process to model the pull via the nuchal ligament. Additional focus was laid on the peculiar shape of the first thoracic vertebra in giraffes. We hypothesized that a habitually upright neck posture should be reflected in the greater ability to withstand compressive loads compared to tensile loads, whereas for species with a habitually suspended posture it should be the opposite. In comparison to species with a suspended posture, species with an upright posture exhibited lower stress (except Giraffidae). For compressive loads in larger species, stress surprisingly increased. Tensile loads in larger species resulted in decreased stress only in species with an intermediate or suspensory neck posture. High stress under tensile loads was mainly reflecting the relative length of the spinous process, while high stress under compressive loads was common in more "bell"-shaped vertebral bodies. The data supports a stability-mobility trade-off at the cervico-thoracic transition in giraffes. Performance under load at the cervico-thoracic boundary is indicative of habitual neck posture and is influenced by body size.

Correlations between local geoclimatic variables and hatchling body size in the sea turtles Caretta caretta and Chelonia mydas.

It has been widely demonstrated that air and sand temperatures influence the anatomy of sea turtle hatchlings. We examined the impact of precipitation during the nesting season on the hatchling body size of loggerhead and green turtles from 37 beaches worldwide. Longitudinal data collected between 2012 and 2018 from Florida (US) and from a sample on Bõa Vista Island (Cabo Verde) carried out in 2019 showed that loggerhead body size at hatching was negatively correlated with precipitation, while precipitation was not correlated with hatchling body size in green turtles. A meta-analysis revealed that precipitation is positively correlated with hatchling mass in loggerhead turtles, while it is positively correlated with straight carapace length and width in green turtle hatchlings. The strongest influence of precipitation was found in the middle of the incubation period of loggerhead turtles in Cabo Verde, and we posit that this is due to an increase in the uptake of water for embryonic growth. These findings highlight the great importance of understanding the correlated effects of regional environmental variables, such as precipitation, on the development of sea turtle hatchlings and will have an impact on the evaluation of ongoing conservation and climate change discussions.

Linking morphology, performance, and habitat utilization: adaptation across biologically relevant 'levels' in tamarins.

BACKGROUND: Biological adaptation manifests itself at the interface of different biologically relevant 'levels', such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these 'levels'. RESULTS: We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons. We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax, based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two. CONCLUSION: This study demonstrates the complex ways in which behavioral and morphological 'levels' map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.

Adjustments of global and local hindlimb properties during terrestrial locomotion of the common quail (Coturnix coturnix).

Previous research has resulted in increasing insight into neuro-mechanical control strategies during perturbed locomotion. In contrast, more general analyses on simple model (template)-related parameters during avian terrestrial locomotion are still rare. Quail kinematic data obtained using X-ray videography combined with ground reaction force measurements were used as a basis to investigate how 'global' template and 'local' leg joint parameters in this small, predominantly terrestrial bird change with speed and gait. Globally, quail locomotion approximates a spring-like behavior in all investigated gaits. However, ground reaction forces are more vertically oriented, which may help to balance the trunk. At the joint level, practically all the spring-like work was found to occur in the intertarsal joint (ITJ). From walking to grounded running, the local stiffness of the ITJ decreases similarly to the reduction observed in global leg stiffness. Thus, in gaits without aerial phases the quails may modulate ITJ stiffness to regulate global leg stiffness, and therefore gait changes, to a significant degree. At higher speeds both global leg compression and stiffness are increased (the latter to values not significantly different to those obtained during walking). This enables the animals to shorten contact time and to generate aerial phases (running). However, we did not observe a change in the stiffness in the ITJ with a change of gait from grounded running to running. We hypothesize that a more extended leg at touch-down, controlled by the joint angles in the knee and ITJ, has an important influence in the leg stiffness adjustment process during running.