Gary B. Gillis

Losing stability: tail loss and jumping in the arboreal lizard Anolis carolinensis

SUMMARY Voluntary loss of an appendage, or autotomy, is a remarkable behavior that is widespread among many arthropods and lower vertebrates. Its immediate benefit, generally escape from a predator, is balanced by various costs, including impaired locomotor performance, reproductive success and long-term survival. Among vertebrates, autotomy is most widespread in lizards, in which tail loss has been documented in close to 100 species. Despite numerous studies of the potential costs of tail autotomy in lizards, none have focused on the importance of the tail in jumping. Using high-speed video we recorded jumps from six lizards (Anolis carolinensis) both before and after removing 80% of the tail to test the hypothesis that tail loss has a significant effect on jumping kinematics. Several key performance metrics, including jump distance and takeoff velocity, were not affected by experimental tail removal, averaging 21 cm and 124 cm s–1, respectively, in both tailed and tailless lizards. However, in-air stability during jumping was greatly compromised after tail removal. Lizards without tails rotated posteriorly more than 30 deg., on average, between takeoff and landing (and sometimes more than 90 deg.) compared with an average of 5 deg. of rotation in lizards with intact tails. Such exaggerated posterior rotation prevents coordinated landing, which is critical for animals that spend much of their time jumping to and from small branches. This work augments recent experiments demonstrating the importance of the tail as a mid-air stabilizer during falling in geckos, and emphasizes new and severe functional costs associated with tail autotomy in arboreal lizards.

Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion

SUMMARY Unlike homologous muscles in many vertebrates, which appear to function similarly during a particular mode of locomotion (e.g. red muscle in swimming fish, pectoralis muscle in flying birds, limb extensors in jumping and swimming frogs), a major knee extensor in mammalian quadrupeds, the vastus lateralis, appears to operate differently in different species studied to date. In rats, the vastus undergoes more stretching early in stance than shortening in later stance. In dogs, the reverse is true; more substantial shortening follows small amounts of initial stretching. And in horses, while the vastus strain trajectory is complex, it is characterized mainly by shortening during stance. In this study, we use sonomicrometry and electromyography to study the vastus lateralis and biceps femoris of goats, with three goals in mind: (1) to see how these muscles work in comparison to homologous muscles studied previously in other taxa; (2) to address how speed and gait impact muscle actions and (3) to test whether fascicles in different parts of the same muscle undergo similar length changes. Results indicate that the biceps femoris undergoes substantial shortening through much of stance, with higher strains in walking and trotting [32–33% resting length (L0)] than galloping (22% L0). These length changes occur with increasing biceps EMG intensities as animals increase speed from walking to galloping. The vastus undergoes a stretch–shorten cycle during stance. Stretching strains are higher during galloping (15% L0) than walking and trotting (9% L0). Shortening strains follow a reverse pattern and are greatest in walking (24% L0), intermediate in trotting (20% L0) and lowest during galloping (17% L0). As a result, the ratio of stretching to shortening increases from below 0.5 in walking and trotting to near 1.0 during galloping. This increasing ratio suggests that the vastus does relatively more positive work than energy absorption at the slower speeds compared with galloping, although an understanding of the timing and magnitude of force production is required to confirm this. Length-change regimes in proximal, middle and distal sites of the vastus are generally comparable, suggesting strain homogeneity through the muscle. When strain rates are compared across taxa, vastus shortening velocities exhibit the scaling pattern predicted by theoretical and empirical work: fascicles shorten relatively faster in smaller animals than larger animals (strain rates near 2 L s–1 have been reported for trotting dogs and were found here for goats, versus 0.6–0.8 L s–1 reported in horses). Interestingly, biceps shortening strain rates are very similar in both goats and rats during walking (1–1.5 L s–1) and trotting (1.5–2.5 L s–1, depending on speed of trot), suggesting that the ratio of in vivo shortening velocities (V) to maximum shortening velocities (Vmax) is smaller in small animals (because of their higher Vmax).

Do toads have a jump on how far they hop? Pre-landing activity timing and intensity in forelimb muscles of hopping Bufo marinus

During jumping or falling in humans and various other mammals, limb muscles are activated before landing, and the intensity and timing of this pre-landing activity are scaled to the expected impact. In this study, we test whether similarly tuned anticipatory muscle activity is present in hopping cane toads. Toads use their forelimbs for landing, and we analysed pre-landing electromyographic (EMG) timing and intensity in relation to hop distance for the m. coracoradialis and m. anconeus, which act antagonistically at the elbow, and are presumably important in stabilizing the forelimb during landing. In most cases, a significant, positive relationship between hop distance and pre-landing EMG intensity was found. Moreover, pre-landing activation timing of m. anconeus was tightly linked to when the forelimbs touched down at landing. Thus, like mammals, toads appear to gauge the timing and magnitude of their impending impact and activate elbow muscles accordingly. To our knowledge these data represent the first demonstration of tuned pre-landing muscle recruitment in anurans and raise questions about how important the visual, vestibular and/or proprioceptive systems are in mediating this response.

A Brief History of Vertebrate Functional Morphology

Abstract The discipline of functional morphology grew out of a comparative anatomical tradition, its transformation into a modern experimental science facilitated largely by technological advances. Early morphologists, such as Cuvier, felt that function was predictable from organismal form, to the extent that animals and plants represented perfect adaptations to their habits. However, anatomy alone could not reveal how organisms actually performed their activities. Recording techniques capable of capturing fast motion were first required to begin to understand animal movement. Muybridge is most famous for his pioneering work in fast photography in the late 19th century, enabling him to “freeze” images of even the fastest horse at a full gallop. In fact, contemporary kinematic analysis grew directly out of the techniques Muybridge developed. Marey made perhaps an even greater contribution to experimental science through his invention of automatic apparati for recording events of animal motion. Over the first half of the 20th century, scientists developed practical methods to record activity patterns from muscles of a living, behaving human or animal. The technique of electromyography, initially used in clinical applications, was co-opted as a tool of organismal biologists in the late 1960s. Comparative anatomy, kinematic analysis and electromyography have for many years been the mainstay of vertebrate functional morphology; however, those interested in animal form and function have recently begun branching out to incorporate approaches from experimental biomechanics and other disciplines (see accompanying symposium papers), and functional morphology now stands at the threshold of becoming a truly integrative, central field in organismal biology.

Loading effects on jump performance in green anole lizards, Anolis carolinensis

SUMMARY Locomotor performance is a crucial determinant of organismal fitness but is often impaired in certain circumstances, such as increased mass (loading) resulting from feeding or gravidity. Although the effects of loading have been studied extensively for striding locomotion, its effects on jumping are poorly understood. Jumping is a mode of locomotion that is widely used across animal taxa. It demands large amounts of power over a short time interval and, consequently, may be affected by loading to a greater extent than other modes of locomotion. We placed artificial loads equal to 30% body mass on individuals of the species Anolis carolinensis to simulate the mass gain following the consumption of a large meal. We investigated the effects of loading on jump performance (maximum jump distance and accuracy), kinematics and power output. Loading caused a significant 18% decline in maximum jump distance and a significant 10% decline in takeoff speed. In other words, the presence of the load caused the lizards to take shorter and slower jumps, whereas takeoff angle and takeoff duration were not affected. By contrast, jump accuracy was unaffected by loading, although accuracy declined when lizards jumped to farther perches. Finally, mass-specific power output did not increase significantly when lizards jumped with loads, suggesting that the ability to produce mechanical power may be a key limiting factor for maximum jump performance. Our results suggest that mass gain after a large meal can pose a significant locomotor challenge and also imply a tradeoff between fulfilling energy requirement and moving efficiently in the environment.

Hopping isn't always about the legs: forelimb muscle activity patterns during toad locomotion.

Although toads are not known for their jumping ability, they are excellent at landing, using their forelimbs to stabilize and decelerate the body as they transition between hops. Forelimb muscles must play important roles during this landing behavior, but to date our understanding of forelimb muscle function during jumping in anurans, particularly after takeoff, is quite limited. Here, we use simultaneous high-speed video and electromyography to characterize the timing and intensity of electrical activity patterns of six muscles that act at the shoulder or elbow joints in the cane toad, Bufo marinus. In particular, we aim to address the importance of these muscles with respect to various potential roles during hopping (e.g. contributing to propulsion during takeoff, resisting impact forces during landing). Five of the six recorded muscles exhibited their highest average intensities during the aerial phase of the hop, with the most intense activity present near forelimb touchdown. In contrast, no muscles exhibited high levels of activity in the initial phase of takeoff. We interpret these data to indicate that the forelimb muscles studied here are likely unimportant in augmenting force production during takeoff, but are critical for both mid-air forelimb positioning and resisting the forces associated with impact. The onset timing of elbow extensors seems to occur at a nearly fixed interval before impact, regardless of hop length, suggesting that these muscles are particularly tuned to resisting impact.

Biomechanics and Control of Landing in Toads

Anything that jumps must land, but unlike during jumping when muscles produce energy to accelerate the body into the air, controlled landing requires muscles to dissipate energy and decelerate the body. Among anurans, toads (genus Bufo) exhibit highly coordinated landing behaviors, using their forelimbs to stabilize the body after touch-down as they lower their hindlimbs to the ground. Moreover, toads land frequently, as they cover distances by stringing together long series of relatively short hops. We have been using toads as a model to understand the biomechanics and motor control strategies of coordinated landing. Our results show that toads prepare for landing differently depending on how far they hop. For example, the forelimbs are extended farther prior to impact after long hops than after short ones. Such kinematic alterations are mirrored by predictable modulation of the recruitment intensity of forelimb muscles before impact, such that longer hops lead to higher levels of pre-landing recruitment of muscles. These differences in kinematics and muscular activity help to control the most flexed configuration of the elbow that is achieved after impact, which in turn constrains the extent to which muscles involved in dissipating energy are stretched. Indeed, a combination of in vivo and in vitro experiments has shown that the elbow-extending anconeus muscle, which is stretched during landing as the elbow flexes, rarely reaches lengths longer than those on the plateau of the muscles length-tension curve (where damage becomes more likely). We have also been studying how movements of the hindlimbs after take-off help to stabilize animals during landing. In particular, the immediate and rapid flexion of a toads knees after take-off leads to a repositioning of the animals center of mass (COM) that better aligns it with ground-reaction forces (GRFs) at impact and reduces torques that would destabilize the animal. Finally, recent work on sensory feedback involved in preparation for landing demonstrates that vision is not required for coordinated landing. Toads can effectively utilize proprioceptive and/or vestibular information during take-off to help inform themselves about landing conditions, but may also use other sensory modalities after take-off to modulate landing behavior.

Total recoil: perch compliance alters jumping performance and kinematics in green anole lizards (Anolis carolinensis).

SUMMARY Jumping is a common form of locomotion for many arboreal animals. Many species of the arboreal lizard genus Anolis occupy habitats in which they must jump to and from unsteady perches, e.g. narrow branches, vines, grass and leaves. Anoles therefore often use compliant perches that could alter jump performance. In this study we conducted a small survey of the compliance of perches used by the arboreal green anole Anolis carolinensis in the wild (N=54 perches) and then, using perches within the range of compliances used by this species, investigated how perch compliance (flexibility) affects the key jumping variables jump distance, takeoff duration, takeoff angle, takeoff speed and landing angle in A. carolinensis in the laboratory (N=11). We observed that lizards lost contact with compliant horizontal perches prior to perch recoil, and increased perch compliance resulted in decreased jump distance and takeoff speed, likely because of the loss of kinetic energy to the flexion of the perch. However, the most striking effect of perch compliance was an unexpected one; perch recoil following takeoff resulted in the lizards being struck on the tail by the perch, even on the narrowest perches. This interaction between the perch and the tail significantly altered body positioning during flight and landing. These results suggest that although the use of compliant perches in the wild is common for this species, jumping from these perches is potentially costly and may affect survival and behavior, particularly in the largest individuals.

Indirect evidence for elastic energy playing a role in limb recovery during toad hopping

Elastic energy is critical for amplifying muscle power during the propulsive phase of anuran jumping. In this study, we use toads (Bufo marinus) to address whether elastic recoil is also involved after take-off to help flex the limbs before landing. The potential for such spring-like behaviour stems from the unusually flexed configuration of a toads hindlimbs in a relaxed state. Manual extension of the knee beyond approximately 90° leads to the rapid development of passive tension in the limb as underlying elastic tissues become stretched. We hypothesized that during take-off, the knee regularly extends beyond this, allowing passive recoil to help drive limb flexion in mid-air. To test this, we used high-speed video and electromyography to record hindlimb kinematics and electrical activity in a hindlimb extensor (semimembranosus) and flexor (iliofibularis). We predicted that hops in which the knees extended further during take-off would require less knee flexor recruitment during recovery. Knees extended beyond 90° in over 80% of hops, and longer hops involved greater degrees of knee extension during take-off and more intense semimembranosus activity. However, knee flexion velocities during recovery were maintained despite a significant decrease in iliofibularis intensity in longer hops, results consistent with elastic recoil playing a role.

The Impact of Tail Loss on Stability during Jumping in Green Anoles (Anolis carolinensis)

Lizards that undergo caudal autotomy experience a variety of consequences, including decreased locomotor performance in a number of cases. One mode of locomotion common to many arboreal lizard species is jumping, and yet little is known about the effects of autotomy on this locomotor mode. In this article we review recent literature demonstrating the importance of the lizard tail as an in-air stabilizer. First, we review work highlighting how a variety of lizards from diverse families can use their tails to control body position in midair. We then move on to cover recent work demonstrating how in at least one species, Anolis carolinensis, tail loss can lead to remarkable instabilities after takeoff during jumping. Such instabilities occur even when animals are jumping toward specific targets both below and above them, although individual variation in the response to tail loss is considerable. Finally, we report results from a study examining whether increased jumping experience after autotomy facilitates the recovery of in-air stability during jumping. Our work suggests it does not, at least not consistently after 5 wk, indicating that any fitness consequences associated with decreased jumping stability are likely to be long term.