Behaviour and muscle activity across the aquatic-terrestrial transition in Polypterus senegalus.

Amphibious fishes moving from water to land experience continuous changes in environmental forces. How these subtle changes impact behavioural transitions cannot be resolved by comparisons of aquatic and terrestrial locomotion. For example, aquatic and terrestrial locomotion appear distinct in the actinopterygian fish Polypterus senegalus; however, it is unclear how gradual water level changes influence the transition between these locomotor behaviours. We tested the hypothesis in P. senegalus that swimming and walking are part of an incremental continuum of behaviour and muscle activity across the environmental transition from water to land rather than two discrete behaviours, as proposed by previous literature. We exposed P. senegalus to discrete environments from fully aquatic to fully terrestrial while recording body and pectoral fin kinematics and muscle activity. Anterior axial red muscle effort increases as water depth decreases; however, a typical swimming-like anterior-to-posterior wave of axial red muscle activity is always present, even during terrestrial locomotion, indicating gradual motor control changes. Thus, walking appears to be based on swimming-like axial muscle activity whereas kinematic differences between swimming and walking appear to be due to mechanical constraints. A discrete change in left-right pectoral fin coordination from in-phase to out-of-phase at 0.7 body depths relies on adductor muscle activity with a similar duty factor and adductor muscle effort that increases gradually as water depth decreases. Thus, despite distinct changes in kinematic timing, neuromuscular patterning is similar across the water depth continuum. As the observed, gradual increases in axial muscle effort reflect muscle activity changes between aquatic and terrestrial environments observed in other elongate fishes, a modified, swimming-like axial muscle activity pattern for terrestrial locomotion may be common among elongate amphibious fishes.

Fin and body neuromuscular coordination changes during walking and swimming in Polypterus senegalus.

The ability to modulate the function of muscle is integral to an animal's ability to function effectively in the face of widely disparate challenges. This modulation of function can manifest through short-term changes in neuromuscular control, but also through long-term changes in force profiles, fatiguability and architecture. However, the relative extent to which shorter-term modulation and longer-term plasticity govern locomotor flexibility remains unclear. Here, we obtain simultaneously recorded kinematic and muscle activity data of fin and body musculature of an amphibious fish, Polypterus senegalus After examining swimming and walking behaviour in aquatically raised individuals, we show that walking behaviour is characterized by greater absolute duration of muscle activity in most muscles when compared with swimming, but that the magnitude of recruitment during walking is only increased in the secondary bursts of fin muscle and in the primary burst of the mid-body point. This localized increase in intensity suggests that walking in P. senegalus is powered in a few key locations on the fish, contrasting with the more distributed, low intensity muscle force that characterizes the stroke cycle during swimming. Finally, the increased intensity in secondary, but not primary, bursts of the fin muscles when walking probably underscores the importance of antagonistic muscle activity to prevent fin collapse, add stabilization and increase body support. Understanding the principles that underlie the flexibility of muscle function can provide key insights into the sources of animal functional and behavioural diversity.

Integrating gastrocnemius force-length properties, in vivo activation and operating lengths reveals how Anolis deal with ecological challenges.

A central question in biology is how animals successfully behave under complex natural conditions. Although changes in locomotor behaviour, motor control and force production in relation to incline are commonly examined, a wide range of other factors, including a range of perch diameters, pervades arboreal habitats. Moving on different substrate diameters requires considerable alteration of body and limb posture, probably causing significant shifts in the lengths of the muscle-tendon units powering locomotion. Thus, how substrate shape impacts in vivo muscle function remains an important but neglected question in ecophysiology. Here, we used high-speed videography, electromyography, in situ contractile experiments and morphology to examine gastrocnemius muscle function during arboreal locomotion in the Cuban knight anole, Anolis equestris The gastrocnemius contributes more to the propulsive effort on broad surfaces than on narrow surfaces. Surprisingly, substrate inclination affected the relationship between the maximum potential force and fibre recruitment; the trade-off that was present between these variables on horizontal surfaces became a positive relationship on inclined surfaces. Finally, the biarticular nature of the gastrocnemius allows it to generate force isometrically, regardless of substrate diameter and incline, despite the fact that the tendons are incapable of stretching during cyclical locomotion. Our results emphasize the importance of considering ecology and muscle function together, and the necessity of examining both mechanical and physiological properties of muscles to understand how animals move in their environment.

Context-dependent changes in motor control and kinematics during locomotion: modulation and decoupling.

Successful locomotion through complex, heterogeneous environments requires the muscles that power locomotion to function effectively under a wide variety of conditions. Although considerable data exist on how animals modulate both kinematics and motor pattern when confronted with orientation (i.e. incline) demands, little is known about the modulation of muscle function in response to changes in structural demands like substrate diameter, compliance and texture. Here, we used high-speed videography and electromyography to examine how substrate incline and perch diameter affected the kinematics and muscle function of both the forelimb and hindlimb in the green anole (Anolis carolinensis). Surprisingly, we found a decoupling of the modulation of kinematics and motor activity, with kinematics being more affected by perch diameter than by incline, and muscle function being more affected by incline than by perch diameter. Also, muscle activity was most stereotyped on the broad, vertical condition, suggesting that, despite being classified as a trunk-crown ecomorph, this species may prefer trunks. These data emphasize the complex interactions between the processes that underlie animal movement and the importance of examining muscle function when considering both the evolution of locomotion and the impacts of ecology on function.

How forelimb and hindlimb function changes with incline and perch diameter in the green anole, Anolis carolinensis.

The range of inclines and perch diameters in arboreal habitats poses a number of functional challenges for locomotion. To effectively overcome these challenges, arboreal lizards execute complex locomotor behaviors involving both the forelimbs and the hindlimbs. However, few studies have examined the role of forelimbs in lizard locomotion. To characterize how the forelimbs and hindlimbs differentially respond to changes in substrate diameter and incline, we obtained three-dimensional high-speed video of green anoles (Anolis carolinensis) running on flat (9 cm wide) and narrow (1.3 cm) perches inclined at 0, 45 and 90 deg. Changes in perch diameter had a greater effect on kinematics than changes in incline, and proximal limb variables were primarily responsible for these kinematic changes. In addition, a number of joint angles exhibited greater excursions on the 45 deg incline compared with the other inclines. Anolis carolinensis adopted strategies to maintain stability similar to those of other arboreal vertebrates, increasing limb flexion, stride frequency and duty factor. However, the humerus and femur exhibited several opposite kinematic trends with changes in perch diameter. Further, the humerus exhibited a greater range of motion than the femur. A combination of anatomy and behavior resulted in differential kinematics between the forelimb and the hindlimb, and also a potential shift in the propulsive mechanism with changes in external demand. This suggests that a better understanding of single limb function comes from an assessment of both forelimbs and hindlimbs. Characterizing forelimb and hindlimb movements may reveal interesting functional differences between Anolis ecomorphs. Investigations into the physiological mechanisms underlying the functional differences between the forelimb and the hindlimb are needed to fully understand how arboreal animals move in complex habitats.