Modern three-dimensional digital methods for studying locomotor biomechanics in tetrapods.

Here, we review the modern interface of three-dimensional (3D) empirical (e.g. motion capture) and theoretical (e.g. modelling and simulation) approaches to the study of terrestrial locomotion using appendages in tetrapod vertebrates. These tools span a spectrum from more empirical approaches such as XROMM, to potentially more intermediate approaches such as finite element analysis, to more theoretical approaches such as dynamic musculoskeletal simulations or conceptual models. These methods have much in common beyond the importance of 3D digital technologies, and are powerfully synergistic when integrated, opening a wide range of hypotheses that can be tested. We discuss the pitfalls and challenges of these 3D methods, leading to consideration of the problems and potential in their current and future usage. The tools (hardware and software) and approaches (e.g. methods for using hardware and software) in the 3D analysis of tetrapod locomotion have matured to the point where now we can use this integration to answer questions we could never have tackled 20 years ago, and apply insights gleaned from them to other fields.

Competing Models of Work in Quadrupedal Walking: Center of Mass Work is Insufficient to Explain Stereotypical Gait.

The walking gaits of cursorial quadrupedal mammals tend to be highly stereotyped as a four-beat pattern with interspersed periods of double and triple stance, often with double-hump ground reaction force profiles. This pattern has long been associated with high energetic economy, due to low apparent work. However, there are differing ways of approximating the work performed during walking and, consequently, different interpretations of the primary mechanism leading to high economy. A focus on Net Center of Mass (COM) Work led to the claim that quadrupedal walking is efficient because it effectively trades potential and kinetic energy of the COM. Individual Limbs COM Work instead focuses on the ability of the limbs to manage the trajectory of the COM to limit energetic losses to the ground ("collisions"). By focusing on the COM, both these metrics effectively dismiss the importance of rotation of the elongate quadrupedal body. Limb Extension Work considers work required to extend and contract each limb like a strut, and accounts for the work of body pitching. We tested the prescriptive ability of these approximations of work by optimizing them within a quadrupedal model with two approximations of the body as a point-mass or a rigid distributed mass. Perfect potential-kinetic energy exchange of the COM was possible when optimizing Net COM Work, resulting in highly compliant gaits with duty factors close to one, far different than observed mammalian gaits. Optimizing Individual Limbs COM Work resulted in alternating periods of single limb stance. Only the distributed mass model, with Limb Extension Work as the cost, resulted in a solution similar to the stereotypical mammalian gait. These results suggest that maintaining a near-constant limb length, with distributed contacts, are more important mechanisms of economy than either transduction of potential-kinetic energy or COM collision mitigation for quadrupedal walking.

The Murphy number: how pitch moment of inertia dictates quadrupedal walking and running energetics.

Many quadrupedal mammals transition from a four-beat walk to a two-beat run (e.g. trot), but some transition to a four-beat run (e.g. amble). Recent analysis shows that a two-beat run minimizes work only for animals with a small pitch moment of inertia (MOI), though empirical MOI were not reported. It was also unclear whether MOI affects gait energetics at slow speeds. Here, I show that a particular normalization of the pitch moment of inertia (the Murphy number) has opposite effects on walking and running energetics. During walking, simultaneous forelimb and hindlimb contacts dampen pitching energy, favouring a four-beat gait that can distribute expensive transfer of support. However, the required pitching of a four-beat walk becomes more expensive as Murphy number increases. Using trajectory optimization of a simple model, I show that both the walking and slow running strategies used by dogs, horses, giraffes and elephants can be explained by work optimization under their specific Murphy numbers. Rotational dynamics have been largely ignored in quadrupedal locomotion, but appear to be a central factor in gait selection.

Estimating Gaits of an Ancient Crocodile-Line Archosaur Through Trajectory Optimization, With Comparison to Fossil Trackways.

Fossil trackways provide a glimpse into the behavior of extinct animals. However, while providing information of the trackmaker size, stride, and even speed, the actual gait of the organism can be ambiguous. This is especially true of quadrupedal animals, where disparate gaits can have similar trackway patterns. Here, predictive simulation using trajectory optimization can help distinguish gaits used by trackmakers. First, we demonstrated that a planar, five-link quadrupedal biomechanical model can generate the qualitative trackway patterns made by domestic dogs, although a systematic error emerges in the track phase (relative distance between ipsilateral pes and manus prints). Next, we used trackway dimensions as inputs to a model of Batrachotomus kupferzellensis, a long-limbed, crocodile-line archosaur (clade Pseudosuchia) from the Middle Triassic of Germany. We found energetically optimal gaits and compared their predicted track phases to those of fossil trackways of Isochirotherium and Brachychirotherium. The optimal results agree with trackways at slow speeds but differ at faster speeds. However, all simulations point to a gait transition around a non-dimensional speed of 0.4 and another at 1.0. The trackways likewise exhibit stark differences in the track phase at these speeds. In all cases, including when simulations are constrained to the fossil track phase, the optimal simulations after the first gait transition do not correspond to a trot, as often used by living crocodiles. Instead, they are a diagonal sequence gait similar to the slow tölt of Icelandic horses. This is the first evidence that extinct pseudosuchians may have exhibited different gaits than their modern relatives and of a gait transition in an extinct pseudosuchian. The results of this analysis highlight areas where the models can be improved to generate more reliable predictions for fossil data while also showcasing how simple models can generate insights about the behavior of extinct animals.

An inelastic quadrupedal model discovers four-beat walking, two-beat running, and pseudo-elastic actuation as energetically optimal.

It is widely held that quadrupeds choose steady gaits that minimize their energetic cost of transport, but it is difficult to explore the entire range of possible footfall sequences empirically. We present a simple model of a quadruped that can spontaneously produce any of the thousands of planar footfall sequences available to quadrupeds. The inelastic, planar model consists of two point masses connected with a rigid trunk on massless legs. It requires only center of mass position, hind and forelimb proportions and a stride-length to speed relationship as input. Through trajectory optimization of a work and force-rate cost, and a large sample of random initial guesses, we provide evidence for the global optimality of symmetrical four-beat walking at low speeds and two beat running (trotting) at intermediate speeds. Using input parameters based on measurements in dogs (Canis lupus familiaris), the model predicts the correct phase offset in walking and a realistic walk-trot transition speed. It also spontaneously reproduces the double-hump ground reaction force profile observed in walking, and the smooth single-hump profile observed in trotting. Actuation appears elastic, despite the model's lack of springs, suggesting that spring-like locomotory behaviour emerges as an optimal tradeoff between work minimization and force-rate penalties.

Reducing gravity takes the bounce out of running.

In gravity below Earth-normal, a person should be able to take higher leaps in running. We asked 10 subjects to run on a treadmill in five levels of simulated reduced gravity and optically tracked centre-of-mass kinematics. Subjects consistently reduced ballistic height compared with running in normal gravity. We explain this trend by considering the vertical take-off velocity (defined as maximum vertical velocity). Energetically optimal gaits should balance the energetic costs of ground-contact collisions (favouring lower take-off velocity), and step frequency penalties such as leg swing work (favouring higher take-off velocity, but less so in reduced gravity). Measured vertical take-off velocity scaled with the square root of gravitational acceleration, following energetic optimality predictions and explaining why ballistic height decreases in lower gravity. The success of work-based costs in predicting this behaviour challenges the notion that gait adaptation in reduced gravity results from an unloading of the stance phase. Only the relationship between take-off velocity and swing cost changes in reduced gravity; the energetic cost of the down-to-up transition for a given vertical take-off velocity does not change with gravity. Because lower gravity allows an elongated swing phase for a given take-off velocity, the motor control system can relax the vertical momentum change in the stance phase, thus reducing ballistic height, without great energetic penalty to leg swing work. Although it may seem counterintuitive, using less 'bouncy' gaits in reduced gravity is a strategy to reduce energetic costs, to which humans seem extremely sensitive.

A Mathematical Model to Capture Complex Microstructure Orientation on Insect Wings.

Microstructures on insect wings can promote directional drop shedding, and the local orientation of these structures is expected to facilitate drop removal. However, microstructures may exhibit very different orientations at different locations on the wing. Using the march fly Penthetria heteroptera, we propose that local orientation of small hairs (microtrichia) reflects a balance of three nonexclusive strategies: (1) preventing water from becoming stuck in intervenous grooves (microtrichia point upslope), (2) shedding water off the wing as readily as possible (microtrichia point towards the nearest edge), and, (3) shedding water away from the body (microtrichia point distally). We present evidence for all three and show that local microtrichial orientation is seldom determined by any one factor. We develop a mathematical model that employs factor-specific weighting values determined via optimization. Our predictions are tested against the orientation of microtrichia randomly sampled from a P. heteroptera specimen. Using the best-fit weighting parameters, the model displays a median residual of 20°; no residual is greater than 46°. The model also reproduces qualitative aspects of microtrichial orientation, such as bifurcation midway between veins and convergence toward peaks. This strong correspondence between modelled and observed orientation supports the role of microtrichia as directional antiwetting devices and highlights the importance of considering both function and wing geometry to explain the organization of natural microstructure arrays.