The economy of terrestrial locomotion.

All else being equal, evolution is going to drive animals to require the least food to move a unit distance. What is the best way to do that? Some efficiencies can be 'hard-wired' into the body - the relatively unchanging morphology of the animal. But flexibility is also needed - given the task at hand, state of the body, or state of the external environment, it may be best to dynamically choose an appropriate mode of locomotion. For example, slow walking may be great for searching and foraging, but it won't catch fast moving prey. Similarly, maximum speed gallops may be great for escaping danger, but they preclude eating along the way. This primer summarizes what we know about the determinants of locomotor costs and the strategies animals use to minimize cost. It summarizes key findings across levels of organization, from individual muscles to interactions with other organisms and the environment. At the mid-level of organization we highlight gaits, a particularly interesting topic of inquiry with a rich history. We are in an exciting time for the science of movement because we have more, better tools than ever before for observing and manipulating systems, from the molecular level to herds of animals on the Savannah. Even more importantly, there are so many open, exciting questions to ask.

Tails stabilize landing of gliding geckos crashing head-first into tree trunks.

Animals use diverse solutions to land on vertical surfaces. Here we show the unique landing of the gliding gecko, Hemidactylus platyurus. Our high-speed video footage in the Southeast Asian rainforest capturing the first recorded, subcritical, short-range glides revealed that geckos did not markedly decrease velocity prior to impact. Unlike specialized gliders, geckos crashed head-first with the tree trunk at 6.0 ± 0.9 m/s (~140 body lengths per second) followed by an enormous pitchback of their head and torso 103 ± 34° away from the tree trunk anchored by only their hind limbs and tail. A dynamic mathematical model pointed to the utility of tails for the fall arresting response (FAR) upon landing. We tested predictions by measuring foot forces during landing of a soft, robotic physical model with an active tail reflex triggered by forefoot contact. As in wild animals, greater landing success was found for tailed robots. Experiments showed that longer tails with an active tail reflex resulted in the lower adhesive foot forces necessary for stabilizing successful landings, with a tail shortened to 25% requiring over twice the adhesive foot force.

Mechanisms for Mid-Air Reorientation Using Tail Rotation in Gliding Geckos.

Arboreal animals face numerous challenges when negotiating complex three-dimensional terrain. Directed aerial descent or gliding flight allows for rapid traversal of arboreal environments, but presents control challenges. Some animals, such as birds or gliding squirrels, have specialized structures to modulate aerodynamic forces while airborne. However, many arboreal animals do not possess these specializations but still control posture and orientation in mid-air. One of the largest inertial segments in lizards is their tail. Inertial reorientation can be used to attain postures appropriate for controlled aerial descent. Here, we discuss the role of tail inertia in a range of mid-air reorientation behaviors using experimental data from geckos in combination with mathematical and robotic models. Geckos can self-right in mid-air by tail rotation alone. Equilibrium glide behavior of geckos in a vertical wind tunnel show that they can steer toward a visual stimulus by using rapid, circular tail rotations to control pitch and yaw. Multiple coordinated tail responses appear to be required for the most effective terminal velocity gliding. A mathematical model allows us to explore the relationship between morphology and the capacity for inertial reorientation by conducting sensitivity analyses, and testing control approaches. Robotic models further define the limits of performance and generate new control hypotheses. Such comparative analysis allows predictions about the diversity of performance across lizard morphologies, relative limb proportions, and provides insights into the evolution of aerial behaviors.

Inertial Tail Effects during Righting of Squirrels in Unexpected Falls: From Behavior to Robotics.

Arboreal mammals navigate a highly three dimensional and discontinuous habitat. Among arboreal mammals, squirrels demonstrate impressive agility. In a recent "viral" YouTube video, unsuspecting squirrels were mechanically catapulted off of a track, inducing an initially uncontrolled rotation of the body. Interestingly, they skillfully stabilized themselves using tail motion, which ultimately allowed the squirrels to land successfully. Here we analyze the mechanism by which the squirrels recover from large body angular rates. We analyzed from the video that squirrels first use their tail to help stabilizing their head to visually fix a landing site. Then the tail starts to rotate to help stabilizing the body, preparing themselves for landing. To analyze further the mechanism of this tail use during mid-air, we built a multibody squirrel model and showed the righting strategy based on body inertia moment changes and active angular momentum transfer between axes. To validate the hypothesized strategy, we made a squirrel-like robot and demonstrated a fall-stabilizing experiment. Our results demonstrate that a squirrel's long tail, despite comprising just 3% of body mass, can inertially stabilize a rapidly rotating body. This research contributes to better understanding the importance of long tails for righting mechanisms in animals living in complex environments such as trees.

The effects of slope and branch structure on the locomotion of a specialized arboreal colubrid snake (Boiga irregularis).

The surfaces in arboreal habitats have variable diameters, slopes, and branching structure that pose functional challenges for animal locomotion. Nevertheless, many lineages of snakes have independently evolved arboreality. We tested the effects of arboreal habitat structure on the locomotion of a highly arboreal species, the brown tree snake (Boiga irregularis), moving on seven diameters (0.6-21 cm) of cylinders oriented at three slopes (0°, 45°, 90°) and with or without pegs. Intermediate diameters of horizontal cylinders maximized speed, and some of the large-diameter cylinders without pegs were impassable when they were inclined. With increased slope the snakes were slower, and they changed from using lateral undulation with sliding contact and balancing to concertina locomotion with periodic static gripping. The presence of pegs increased the speeds of the brown tree snakes and resulted in them only using lateral undulation. Surface diameter, slope, and the occurrence of pegs also had widespread significant effects on the kinematics of the brown tree snakes. Overall, compared to anatomically less specialized corn snakes, brown tree snakes use more lateral undulation, are usually much faster, and are able to move on a wider variety of surfaces. Unlike some of the trade-offs found previously between two less specialized species of snakes with different stoutness when they used modes of arboreal locomotion that involved either balancing or gripping, the slender-bodied brown tree snakes excel at both. Hence, this species may not only be a "jack of all trades" but also a master of many.

Gripping during climbing of arboreal snakes may be safe but not economical.

On the steep surfaces that are common in arboreal environments, many types of animals without claws or adhesive structures must use muscular force to generate sufficient normal force to prevent slipping and climb successfully. Unlike many limbed arboreal animals that have discrete gripping regions on the feet, the elongate bodies of snakes allow for considerable modulation of both the size and orientation of the gripping region. We quantified the gripping forces of snakes climbing a vertical cylinder to determine the extent to which their force production favoured economy or safety. Our sample included four boid species and one colubrid. Nearly all of the gripping forces that we observed for each snake exceeded our estimate of the minimum required, and snakes commonly produced more than three times the normal force required to support their body weight. This suggests that a large safety factor to avoid slipping and falling is more important than locomotor economy.

Incline and peg spacing have interactive effects on the arboreal locomotor performance and kinematics of brown tree snakes, Boiga irregularis.

Many animals move using lateral undulations, but snakes are noteworthy for using this type of locomotion in an unusual diversity of environments, including trees in which both the spacing and orientation of branches vary considerably. Despite branches providing discrete locations for snakes to generate propulsive forces during lateral undulation, the consequences of branch spacing for the locomotion of snakes are poorly understood. Hence, we determined maximal speeds and kinematics of an arboreal snake (Boiga irregularis) crawling on horizontal and vertical cylinders with pegs that simulated different spacing between secondary branches. Peg spacing, perch orientation and their two-way interaction term had widespread, significant effects on both performance and kinematics. For the horizontal surfaces, maximal locomotor speed occurred with intermediate peg spacing, and it was nearly twice as fast as for both the smallest and largest peg spacings. By contrast, the locomotor speed of snakes on the vertical surfaces was unaffected by peg spacing, and was uniformly slower than that for the horizontal surfaces. For both perch orientations, the number of pegs touched by the snake decreased as peg spacing increased, and while touching only one peg the snakes crawled with apparent ease and steady speed. The snakes crawled vertically with only one peg as quickly as they did using 2-10 pegs. Pegs on a horizontal cylinder are probably important both for propulsion of snakes and prevention of long-axis rolling, whereas pegs protruding from vertical cylinders and those protruding from horizontal planar surfaces are probably used almost exclusively for propulsion.

The effects of three-dimensional gap orientation on bridging performance and behavior of brown tree snakes (Boiga irregularis).

Traversing gaps with different orientations within arboreal environments has ecological relevance and mechanical consequences for animals. For example, the orientation of the animal while crossing gaps determines whether the torques acting on the body tend to cause it to pitch or roll from the supporting perch or fail as a result of localized bending. The elongate bodies of snakes seem well suited for crossing gaps, but a long unsupported portion of the body can create large torques that make gap bridging demanding. We tested whether the three-dimensional orientation of substrates across a gap affected the performance and behavior of an arboreal snake (Boiga irregularis). The snakes crossed gaps 65% larger for vertical than for horizontal trajectories and 13% greater for straight trajectories than for those with a 90 deg turn within the horizontal plane. Our results suggest that failure due to the inability to keep the body rigid at the edge of the gap may be the primary constraint on performance for gaps with a large horizontal component. In addition, the decreased performance when the destination perch was oriented at an angle to the long axis of the initial perch was probably a result of the inability of snakes to maintain balance due to the large rolling torque. For some very large gaps the snakes enhanced their performance by using rapid lunges to cross otherwise impassable gaps. Perhaps such dynamic movements preceded the aerial behavior observed in other species of arboreal snakes.

Ecological and biomechanical insights into the evolution of gliding in mammals.

Gliding has evolved independently at least six times in mammals. Multiple hypotheses have been proposed to explain the evolution of gliding. These include the evasion of predators, economical locomotion or foraging, control of landing forces, and habitat structure. Here we use a combination of comparative methods and ecological and biomechanical data collected from free-ranging animals to evaluate these hypotheses. Our comparative data suggest that the origins of gliding are often associated with shifts to low-quality diets including leaves and plant exudates. Further, data from free-ranging colugos suggest that although gliding is not more energetically economical than moving through the canopy, it is much faster, allowing shorter times of transit between foraging patches and therefore more time available to forage in a given patch. In addition to moving quickly, gliding mammals spend only a small fraction of their overall time engaged in locomotion, likely offsetting its high cost. Kinetic data for both take-off and landing suggest that selection on these behaviors could also have shaped the evolution of gliding. Glides are initiated by high-velocity leaps that are potentially effective in evading arboreal predators. Further, upon landing, the ability to control aerodynamic forces and reduce velocity prior to impact is likely key to extending distances of leaps or glides while reducing the likelihood of injury. It is unlikely that any one of these hypotheses exclusively explains the evolution of gliding, but by examining gliding in multiple groups of extant animals in ecological and biomechanical contexts, new insights into the evolution of gliding can be gained.

Gliding saves time but not energy in Malayan colugos.

Gliding is thought to be an economical form of locomotion. However, few data on the climbing and gliding of free-ranging gliding mammals are available. This study employed an animal-borne three-dimensional acceleration data-logging system to collect continuous data on the climbing and gliding of free-ranging Malayan colugos, Galeopterus variegatus. We combined these movement data with empirical estimates of the metabolic costs to move horizontally or vertically to test this long-standing hypothesis by determining whether the metabolic cost to climb to sufficient height to glide a given distance was less than the cost to move an equivalent distance horizontally through the canopy. On average, colugos climb a short distance to initiate glides. However, due to the high energetic cost of climbing, gliding is more energetically costly to move a given horizontal distance than would be predicted for an animal travelling the same distance through the canopy. Furthermore, because colugos spend a small fraction of their time engaged in locomotor activity, the high costs have little effect on their overall energy budget. As a result, the energetic economy hypothesis for the origins of gliding is not supported. It is likely that other ecologically relevant factors have played a greater role in the origins of gliding in colugos and other mammals.

Substrate diameter and compliance affect the gripping strategies and locomotor mode of climbing boa constrictors.

Arboreal habitats pose unique challenges for locomotion as a result of their narrow cylindrical surfaces and discontinuities between branches. Decreased diameter of branches increases compliance, which can pose additional challenges, including effects on stability and energy damping. However, the combined effects of substrate diameter and compliance are poorly understood for any animal. We quantified performance, kinematics and substrate deformation while boa constrictors (Boa constrictor) climbed vertical ropes with three diameters (3, 6 and 9 mm) and four tensions (0.5, 1.0, 1.5 and 2.0 body weights). Mean forward velocity decreased significantly with both decreased diameter and increased compliance. Both diameter and compliance had numerous effects on locomotor kinematics, but diameter had larger and more pervasive effects than compliance. Locomotion on the largest diameter had a larger forward excursion per cycle, and the locomotor mode and gripping strategy differed from that on the smaller diameters. On larger diameters, snakes primarily applied opposing forces at the same location on the rope to grip. By contrast, on smaller diameters forces were applied in opposite directions at different locations along the rope, resulting in increased rope deformation. Although energy is likely to be lost during deformation, snakes might use increased surface deformation as a strategy to enhance their ability to grip.

Take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo (Galeopterus variegatus).

Arboreal animals negotiate a highly three-dimensional world that is discontinuous on many spatial scales. As the scale of substrate discontinuity increases, many arboreal animals rely on leaping or gliding locomotion between distant supports. In order to successfully move through their habitat, gliding animals must actively modulate both propulsive and aerodynamic forces. Here we examined the take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo (Galeopterus variegatus) using a custom-designed three-dimensional accelerometry system. We found that colugos increase the propulsive impulse to affect longer glides. However, we also found that landing forces are negatively associated with glide distance. Landing forces decrease rapidly as glide distance increases from the shortest glides, then level off, suggesting that the ability to reorient the aerodynamic forces prior to landing is an important mechanism to reduce velocity and thus landing forces. This ability to substantially alter the aerodynamic forces acting on the patagial wing in order to reorient the body is a key to the transition between leaping and gliding and allows gliding mammals to travel long distances between trees with reduced risk of injury. Longer glides may increase the access to distributed resources and reduce the exposure to predators in the canopy or on the forest floor.