Brandon M. Kilbourne

Morphological Integration Versus Ecological Plasticity in the Avian Pelvic Limb Skeleton

Understanding patterns and distributions of morphological traits is essential for discerning underpinning processes of morphological variation. We report on the variation in the avian pelvic limb skeleton. Length and width variables were measured in the skeletons of 236 avian species in order to examine the importance of body mass, ecological factors, phylogeny and integration in the formation of specific hindlimb morphology. Scaling relationships with body mass were analyzed across Aves and in individual avian subclades. Principal component analysis and multiple regressions were performed to examine the relationship between morphology, ecology, and phylogeny. Finally, the occurrence of within‐limb morphological integration was tested by partial correlation analysis of the residuals from element lengths vs. body mass and correlation analysis of avian hindlimb proportions. Body mass is the greatest contributor to variation, and it strongly influences variation in avian skeletal lengths. Lengthening of the leg typically comes from disproportionate increases in tibiotarsal and tarsometatarsal length. Partial correlation analysis showed that only these two elements are distinctly integrated consistently across all bird taxa, whereas relation of femur and third toe to other limb elements displays no clear pattern. Hence, morphological integration of all elements is not a prerequisite for limb design, and variation between taxa is mainly to be found in femoral and digital length. Furthermore, variation in tibiotarsal relative length is much lower than in other elements likely due to geometric constrains. Clear ecological adaptations are obscured by multifunctionality of the avian hindlimb, and phylogeny significantly constrains the morphology. Finally, when looking at relative lengths segmented limbs meet the requirements of many‐to‐one‐mapping of phenotype to functional property, in line with a common concept of evolvability of function and morphology. J. Morphol., 2013.

Mixed gaits in small avian terrestrial locomotion.

Scientists have historically categorized gaits discretely (e.g. regular gaits such as walking, running). However, previous results suggest that animals such as birds might mix or regularly or stochastically switch between gaits while maintaining a steady locomotor speed. Here, we combined a novel and completely automated large-scale study (over one million frames) on motions of the center of mass in several bird species (quail, oystercatcher, northern lapwing, pigeon, and avocet) with numerical simulations. The birds studied do not strictly prefer walking mechanics at lower speeds or running mechanics at higher speeds. Moreover, our results clearly display that the birds in our study employ mixed gaits (such as one step walking followed by one step using running mechanics) more often than walking and, surprisingly, maybe as often as grounded running. Using a bio-inspired model based on parameters obtained from real quails, we found two types of stable mixed gaits. In the first, both legs exhibit different gait mechanics, whereas in the second, legs gradually alternate from one gait mechanics into the other. Interestingly, mixed gaits parameters mostly overlap those of grounded running. Thus, perturbations or changes in the state induce a switch from grounded running to mixed gaits or vice versa.

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

ABSTRACT Differing limb proportions in terms of length and mass, as well as differences in mass being concentrated proximally or distally, influence the limbs 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 limbs 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. Summary: Shorebird species with higher values of limb rotational inertia flex their limbs more during terrestrial locomotion; swing phase kinematics may therefore be strongly tied to limb rotational inertia.

Minimizing the cost of locomotion with inclined trunk predicts crouched leg kinematics of small birds at realistic levels of elastic recoil

ABSTRACT Small birds move with pronograde trunk orientation and crouched legs. Although the pronograde trunk has been suggested to be beneficial for grounded running, the cause(s) of the specific leg kinematics are unknown. Here we show that three charadriiform bird species (northern lapwing, oystercatcher, and avocet; great examples of closely related species that differ remarkably in their hind limb design) move their leg segments during stance in a way that minimizes the cost of locomotion. We imposed measured trunk motions and ground reaction forces on a kinematic model of the birds. The model was used to search for leg configurations that minimize leg work that accounts for two factors: elastic recoil in the intertarsal joint, and cheaper negative muscle work relative to positive muscle work. A physiological level of elasticity (∼0.6) yielded segment motions that match the experimental data best, with a root mean square of angular deviations of ∼2.1 deg. This finding suggests that the exploitation of elastic recoil shapes the crouched leg kinematics of small birds under the constraint of pronograde trunk motion. Considering that an upright trunk and more extended legs likely decrease the cost of locomotion, our results imply that the cost of locomotion is a secondary movement criterion for small birds. Scaling arguments suggest that our approach may be utilized to provide new insights into the motion of extinct species such as dinosaurs. Summary: Exploitation of elastic recoil shapes the stance phases segment movement in small birds; however, reducing the cost of locomotion is only a secondary movement criterion.

The evolution of locomotor rhythmicity in tetrapods.

Differences in rhythmicity (relative variance in cycle period) among mammal, fish, and lizard feeding systems have been hypothesized to be associated with differences in their sensorimotor control systems. We tested this hypothesis by examining whether the locomotion of tachymetabolic tetrapods (birds and mammals) is more rhythmic than that of bradymetabolic tetrapods (lizards, alligators, turtles, salamanders). Species averages of intraindividual coefficients of variation in cycle period were compared while controlling for gait and substrate. Variance in locomotor cycle periods is significantly lower in tachymetabolic than in bradymetabolic animals for datasets that include treadmill locomotion, non‐treadmill locomotion, or both. When phylogenetic relationships are taken into account the pooled analyses remain significant, whereas the non‐treadmill and the treadmill analyses become nonsignificant. The co‐occurrence of relatively high rhythmicity in both feeding and locomotor systems of tachymetabolic tetrapods suggests that the anatomical substrate of rhythmicity is in the motor control system, not in the musculoskeletal components.

Scale effects and morphological diversification in hindlimb segment mass proportions in neognath birds

IntroductionIn spite of considerable work on the linear proportions of limbs in amniotes, it remains unknown whether differences in scale effects between proximal and distal limb segments has the potential to influence locomotor costs in amniote lineages and how changes in the mass proportions of limbs have factored into amniote diversification. To broaden our understanding of how the mass proportions of limbs vary within amniote lineages, I collected data on hindlimb segment masses – thigh, shank, pes, tarsometatarsal segment, and digits – from 38 species of neognath birds, one of the most speciose amniote clades. I scaled each of these traits against measures of body size (body mass) and hindlimb size (hindlimb length) to test for departures from isometry. Additionally, I applied two parameters of trait evolution (Pagel’s λ and δ) to understand patterns of diversification in hindlimb segment mass in neognaths.ResultsAll segment masses are positively allometric with body mass. Segment masses are isometric with hindlimb length. When examining scale effects in the neognath subclade Land Birds, segment masses were again positively allometric with body mass; however, shank, pedal, and tarsometatarsal segment masses were also positively allometric with hindlimb length. Methods of branch length scaling to detect phylogenetic signal (i.e., Pagel’s λ) and increasing or decreasing rates of trait change over time (i.e., Pagel’s δ) suffer from wide confidence intervals, likely due to small sample size and deep divergence times.ConclusionsThe scaling of segment masses appears to be more strongly related to the scaling of limb bone mass as opposed to length, and the scaling of hindlimb mass distribution is more a function of scale effects in limb posture than proximo-distal differences in the scaling of limb segment mass. Though negative allometry of segment masses appears to be precluded by the need for mechanically sound limbs, the positive allometry of segment masses relative to body mass may underlie scale effects in stride frequency and length between smaller and larger neognaths. While variation in linear proportions of limbs appear to be governed by developmental mechanisms, variation in mass proportions does not appear to be constrained so.

Automated approximation of center of mass position in X-ray sequences of animal locomotion.

A crucial aspect of comparative biomechanical research is the center of mass (CoM) estimation in animal locomotion scenarios. Important applications include the parameter estimation of locomotion models, the discrimination of gaits, or the calculation of mechanical work during locomotion. Several methods exist to approximate the CoM position, e.g. force-plate-based approaches, kinematic approaches, or the reaction board method. However, they all share the drawback of not being suitable for large scale studies, as detailed initial conditions from kinematics are required (force-plates), manual interaction is necessary (kinematic approach), or only static settings can be analyzed (reaction board). For the increasingly popular case of X-ray-based animal locomotion analysis, we present an alternative approach for CoM estimation which overcomes these shortcomings. The main idea is to only use the recorded X-ray images, and to map each pixel to the mass of matter it represents. As a consequence, our approach is surgically noninvasive, independent of animal species and locomotion characteristics, and neither requires prior knowledge nor any kind of user interaction. To assess the quality of our approach, we conducted a comparison to highly accurate reaction board experiments for lapwing and rat cadavers, and achieved an average accuracy of 2.6mm (less than 2% of the animal body length). We additionally verified the practical applicability of the algorithm by comparison to a previously published CoM study which is based on the kinematic method, yielding comparable results.

Manipulated Changes in Limb Mass and Rotational Inertia in Trotting Dogs (Canis lupus familiaris) and Their Effect on Limb Kinematics

While the mass distribution of limbs is known to influence the metabolic energy consumed during locomotion, it remains unknown how the mass distribution of limbs may influence overall limb kinematics and whether the influence of limb mass distribution on limb kinematics differs between fore- and hindlimbs. To examine limb mass distributions influence upon fore- and hindlimb kinematics, temporal stride parameters and swing phase joint kinematics were recorded from four dogs trotting on a treadmill with 0.5% and 1.0% body mass added to each limb, forelimbs alone, and hindlimbs alone, as well as with no added mass. Under all loading conditions, stride period did not differ between fore- and hindlimbs; however, forelimbs exhibited greater duty factors and stance durations, whereas hindlimbs exhibited greater swing durations, which may be related to the hindlimbs greater mass. Changes in forelimb joint and hip range of motion (RoM), flexion, and extension were subject to a high amount of kinematic plasticity among dogs. In contrast, for the knee and ankle, distally loading all four limbs or hindlimbs alone substantially increased joint RoM and flexion. Increased flexion of the knee and ankle has the potential to reduce the hindlimbs rotational inertia during swing phase. The differing response of fore- and hindlimbs with regard to joint kinematics is likely due to differences in their mass and mass distribution and differences in the physiological traits of fore- and hindlimb protractors and joint flexors.