Environmental effects on undulatory locomotion in the American eel Anguilla rostrata: kinematics in water and on land

1998 ◽  
Vol 201 (7) ◽  
pp. 949-961 ◽  
Author(s):  
G. B. Gillis

Historically, the study of swimming eels (genus Anguilla) has been integral to our understanding of the mechanics and muscle activity patterns used by fish to propel themselves in the aquatic environment. However, no quantitative kinematic analysis has been reported for these animals. Additionally, eels are known to make transient terrestrial excursions, and in the past it has been presumed (but never tested) that the patterns of undulatory movement used terrestrially are similar to those used during swimming. In this study, high-speed video was used to characterize the kinematic patterns of undulatory locomotion in water and on land in the American eel Anguilla rostrata. During swimming, eels show a nonlinear increase in the amplitude of lateral undulations along their bodies, reaching an average maximum of 0.08L, where L is total length, at the tip of the tail. However, in contrast to previous observations, the most anterior regions of their bodies do not undergo significant undulation. In addition, a temporal lag (typically 10–15 % of an undulatory cycle) exists between maximal flexion and displacement at any given longitudinal position. Swimming speed does not have a consistent effect on this lag or on the stride length (distance moved per tailbeat) of the animal. Speed does have subtle (although statistically insignificant) effects on the patterns of undulatory amplitude and intervertebral flexion along the body. On land, eels also use lateral undulations to propel themselves; however, their entire bodies are typically bent into waves, and the undulatory amplitude at all body positions is significantly greater than during swimming at equivalent speeds. The temporal lag between flexion and displacement seen during swimming is not present during terrestrial locomotion. While eels cannot move forwards as quickly on land as they do in water, they do increase locomotor speed with increasing tailbeat frequency. The clear kinematic distinctions present between aquatic and terrestrial locomotor sequences suggest that eels might be using different axial muscle activity patterns to locomote in the different environments.

2000 ◽  
Vol 203 (3) ◽  
pp. 471-480 ◽  
Author(s):  
G.B. Gillis

Eels (Anguilla rostrata) are known to make occasional transitory excursions into the terrestrial environment. While on land, their locomotor kinematics deviate drastically from that observed during swimming. In this study, electromyographic (EMG) recordings were made from white muscle at various longitudinal positions in eels performing undulatory locomotion on land to determine the muscle activity patterns underlying these terrestrial movements. As during swimming, eels propagate a wave of muscle activity from anterior to posterior during terrestrial locomotion. However, the intensity of EMG bursts is much greater on land (on average approximately five times greater than in water). In addition, anteriorly located musculature has higher-intensity EMG bursts than posteriorly located muscle during locomotion on land. EMG duty cycle (burst duration relative to undulatory cycle time) is significantly affected by longitudinal position during terrestrial locomotion, and duty cycles are significantly greater on land (0.4-0.5 cycles) than in water (0. 2–0.3 cycles). Finally, as in swimming, a phase shift in the timing of muscle activity exists such that posteriorly located muscle fibers become activated earlier in their strain cycle than do more anteriorly located fibers. However, fibers become activated much later in their muscle strain cycle on land than in water. Therefore, it is clear that, while eels propagate a wave of muscle activity posteriorly to generate backward-traveling waves that generate propulsive thrust both in water and on land, the specific patterns of timing and the intensity of muscle activity are substantially altered depending upon the environment. This suggests that physical differences in an animal's external environment can play a substantial role in affecting the motor control of locomotion, even when similar structures are used to generate the propulsive forces.


2002 ◽  
Vol 205 (17) ◽  
pp. 2591-2603 ◽  
Author(s):  
Eric D. Tytell ◽  
George V. Lauder

SUMMARYThe fast-start escape response is the primary reflexive escape mechanism in a wide phylogenetic range of fishes. To add detail to previously reported novel muscle activity patterns during the escape response of the bichir, Polypterus, we analyzed escape kinematics and muscle activity patterns in Polypterus senegalus using high-speed video and electromyography (EMG). Five fish were filmed at 250 Hz while synchronously recording white muscle activity at five sites on both sides of the body simultaneously (10 sites in total). Body wave speed and center of mass velocity, acceleration and curvature were calculated from digitized outlines. Six EMG variables per channel were also measured to characterize the motor pattern. P. senegalus shows a wide range of activity patterns, from very strong responses, in which the head often touched the tail, to very weak responses. This variation in strength is significantly correlated with the stimulus and is mechanically driven by changes in stage 1 muscle activity duration. Besides these changes in duration, the stage 1 muscle activity is unusual because it has strong bilateral activity, although the observed contralateral activity is significantly weaker and shorter in duration than ipsilateral activity. Bilateral activity may stiffen the body, but it does so by a constant amount over the variation we observed; therefore, P. senegalus does not modulate fast-start wave speed by changing body stiffness. Escape responses almost always have stage 2 contralateral muscle activity, often only in the anterior third of the body. The magnitude of the stage 2 activity is the primary predictor of final escape velocity.


1993 ◽  
Vol 176 (1) ◽  
pp. 55-76 ◽  
Author(s):  
S. M. Gatesy ◽  
K. P. Dial

The electrical activity of major caudal muscles of the pigeon (Columba livia) was recorded during five modes of aerial and terrestrial locomotion. Tail muscle electromyograms were correlated with movement using high-speed cinematography and compared to activity in selected muscles of the wings, legs and trunk. During walking, the pectoralis and most tail muscles are normally inactive, but levator muscle activity alternates with the striding legs. In flight, caudal muscles are phasically active with each wingbeat and undergo distinct changes in electromyographic pattern between liftoff, takeoff, slow level flapping and landing modes. The temporal flexibility of tail muscle activity differs significantly from the stereotypic timing of wing muscles in pigeons performing the same flight modes. These neural programs may represent different solutions to the control of flight surfaces in the rapidly oscillating wing and the relatively stationary caudal skeleton. Birds exhibit a novel alliance of tail and forelimb use during aerial locomotion. We suggest that there is evidence of anatomical and functional decoupling of the tail from adjacent hindlimb and trunk muscles during avian evolution to facilitate its specialization for rectricial control in flight.


2020 ◽  
Vol 60 (1) ◽  
pp. 180-189
Author(s):  
Erica Redmann ◽  
Alina Sheikh ◽  
Areej Alqahtani ◽  
Mica McCarty-Glenn ◽  
Shazrah Syed ◽  
...  

Synopsis Fishes overcome a variety of challenges in order to invade the terrestrial environment. Terrestrial invasions by fish occur over a variety of environmental contexts. In order to advance their bodies on land, fishes capable of terrestrial excursions tend to use one of three different types of locomotor modes: axial-based, appendage-based, or axial-appendage-based. Elongate species with reduced appendages, such as the American eel, Anguilla rostrata, rely on axial based locomotion in water and on land. When eels move from water to land as part of their complex life cycle, they inevitably encounter a variety of substrates and must traverse variable degrees of incline. The aim of this study was to determine the effect of substrate and incline on the terrestrial locomotion of the American eel. In order to do this, eels were filmed from a dorsal view on three substrates and four inclines: sand, loose pebbles, and fixed (glued) pebbles at 0°, 5°, 10°, and 15°. We digitized 20 evenly spaced points along the body to examine the following characteristics of locomotion: velocity, distance ratio (DR), and wave parameters such as wave amplitude, frequency, and length and assessed whether substrate, incline, or body position affected these parameters. DR, our metric of movement efficiency, was highest on the flat sand condition and lowest on 15° pebble conditions. Efficiency also varied across the body. Velocity followed a similar pattern being highest on sand at 0° and lowest at the steepest inclines. Wave amplitude generally increased toward the tail but was similar across substrates and inclines. Wave frequency was relatively consistent across the body on both pebble substrates, but on sand, frequency was higher toward the head but decreased toward the tail. Wavelengths on sand were the longest at 0° near the head and shorter wavelengths were observed on steeper inclines. Both pebble substrates elicited lower wavelengths that were more similar across the body. Overall, A. rostrata were more effective in navigating compliant substrates but struggled at steeper inclines. Our findings provide insight into locomotor challenges that American eels may encounter as they move from and between bodies of water.


1992 ◽  
Vol 162 (1) ◽  
pp. 107-130 ◽  
Author(s):  
LARRY M. FROLICH ◽  
ANDREW A. BIEWENER

Aquatic neotenic and terrestrial metamorphosed salamanders {Ambystoma tigrinum) were videotaped simultaneously with electromyographic (EMG) recording from five epaxial myotomes along the animal's trunk during swimming in a flow tank and trotting on a treadmill to investigate axial function during aquatic and terrestrial locomotion. Neotenic and metamorphosed individuals swim using very similar axial wave patterns, despite significant differences in axial morphology. During swimming, both forms exhibit traveling waves of axial flexion and muscle activity, with an increasing EMG-mechanical delay as these waves travel down the trunk. In contrast to swimming, during trotting metamorphosed individuals exhibit a standing wave of axial flexion produced by synchronous activation of ipsilateral epaxial myotomes along the trunk. Thus, metamorphosed individuals employ two distinct axial motor programs -- one used during swimming and one used during trotting. The transition from a traveling axial wave during swimming to a standing axial wave during trotting in A. tigrinum may be an appropriate analogy for similar transitions in axial locomotor function during theoriginal evolution of terrestriality in early tetrapods.


2001 ◽  
Vol 204 (11) ◽  
pp. 1979-1989 ◽  
Author(s):  
Wallace O. Bennett ◽  
Rachel S. Simons ◽  
Elizabeth L. Brainerd

SUMMARY The function of the lateral hypaxial muscles during locomotion in tetrapods is controversial. Currently, there are two hypotheses of lateral hypaxial muscle function. The first, supported by electromyographic (EMG) data from a lizard (Iguana iguana) and a salamander (Dicamptodon ensatus), suggests that hypaxial muscles function to bend the body during swimming and to resist long-axis torsion during walking. The second, supported by EMG data from lizards during relatively high-speed locomotion, suggests that these muscles function primarily to bend the body during locomotion, not to resist torsional forces. To determine whether the results from D. ensatus hold for another salamander, we recorded lateral hypaxial muscle EMGs synchronized with body and limb kinematics in the tiger salamander Ambystoma tigrinum. In agreement with results from aquatic locomotion in D. ensatus, all four layers of lateral hypaxial musculature were found to show synchronous EMG activity during swimming in A. tigrinum. Our findings for terrestrial locomotion also agree with previous results from D. ensatus and support the torsion resistance hypothesis for terrestrial locomotion. We observed asynchronous EMG bursts of relatively high intensity in the lateral and medial pairs of hypaxial muscles during walking in tiger salamanders (we call these ‘α-bursts’). We infer from this pattern that the more lateral two layers of oblique hypaxial musculature, Mm. obliquus externus superficialis (OES) and obliquus externus profundus (OEP), are active on the side towards which the trunk is bending, while the more medial two layers, Mm. obliquus internus (OI) and transversus abdominis (TA), are active on the opposite side. This result is consistent with the hypothesis proposed for D. ensatus that the OES and OEP generate torsional moments to counteract ground reaction forces generated by forelimb support, while the OI and TA generate torsional moments to counteract ground reaction forces from hindlimb support. However, unlike the EMG pattern reported for D. ensatus, a second, lower-intensity burst of EMG activity (‘β-burst’) was sometimes recorded from the lateral hypaxial muscles in A. tigrinum. As seen in other muscle systems, these β-bursts of hypaxial muscle coactivation may function to provide fine motor control during locomotion. The presence of asynchronous, relatively high-intensity α-bursts indicates that the lateral hypaxial muscles generate torsional moments during terrestrial locomotion, but it is possible that the balance of forces from both α- and β-bursts may allow the lateral hypaxial muscles to contribute to lateral bending of the body as well.


1993 ◽  
Vol 71 (1) ◽  
pp. 189-195 ◽  
Author(s):  
M. A. Kasapi ◽  
P. Domenici ◽  
R. W. Blake ◽  
D. Harper

The kinematics and performance of the escape responses of the knifefish Xenomystus nigri, a fish specialized for low-speed, undulatory median-fin propulsion, were recorded by means of high-speed cinematography. Two types of escape were observed, one involving the formation of a C-shape along the longitudinal axis of the fish (stage 1), followed by a slow recoil of the body (single bend); the other (double bend) involved stage 1 followed by a contralateral bend (stage 2). The pectoral fins were extended throughout escapes of both types. The average maximum acceleration for double bend escapes was 127.98 m∙s−2; acceleration was usually greatest in stage 1. In double bend escapes, turning angles for stages 1 and 2 were not correlated. Pitch and roll orientations change during escapes. In stage 1, the average roll and average pitch were linearly correlated, suggesting that roll was partly responsible for establishing pitch. Knifefish achieved high maximum acceleration relative to other fish. Therefore, performance was not compromised by morphological specialization for low-speed swimming; however, a negative correlation of pitch with acceleration in stage 1 suggested that escapes involve a trade-off between acceleration and confusing a predator by changing planar orientation.


2000 ◽  
Vol 203 (17) ◽  
pp. 2589-2601 ◽  
Author(s):  
B.R. Moon

Snakes are excellent subjects for studying functional versatility and potential constraints because their movements are constrained to vertebral bending and twisting. In many snakes, swallowing is a kind of inside-out locomotion. During swallowing, vertebral bends push food from the jaws along a substantial length of the body to the stomach. In gopher snakes (Pituophis melanoleucus) and king snakes (Lampropeltis getula), swallowing often begins with lateral bending of the head and neck as the jaws advance unilaterally over the prey. Axial movement then shifts to accordion-like, concertina bending as the prey enters the oesophagus. Once the prey is completely engulfed, concertina bending shifts to undulatory bending that pushes the prey to the stomach. The shift from concertina to undulatory bending reflects a shift from pulling the prey into the throat (or advancing the mouth over the prey) to pushing it along the oesophagus towards the stomach. Undulatory kinematics and muscular activity patterns are similar in swallowing and undulatory locomotion. However, the distinct mechanical demands of internal versus external force exertion result in different duty factors of muscle activity. Feeding and locomotor movements are thus integral functions of the snake axial system.


1985 ◽  
Vol 53 (6) ◽  
pp. 1517-1534 ◽  
Author(s):  
G. A. Robertson ◽  
L. I. Mortin ◽  
J. Keifer ◽  
P. S. Stein

A turtle with a complete transection of the spinal cord, termed a spinal turtle, exhibits three types or “forms” of the scratch reflex: the rostral scratch, pocket scratch, and caudal scratch (21). Each scratch form is elicited by tactile stimulation of a site on the body surface innervated by afferents entering the spinal cord caudal to the transection. We recorded electromyographic (EMG) potentials from the hindlimb during each of the three forms of the scratch in the spinal turtle (see Fig. 1). Common to all scratch forms is the rhythmic alternation of the activity of the hip protractor muscle (VP-HP) and hip retractor muscle (HR-KF). Each form of the scratch displays a characteristic timing of the activity of the knee extensor muscle (FT-KE) with respect to the cycle of activity of the hip muscles VP-HP and HR-KF. In a rostral scratch, activation of FT-KE occurs during the latter portion of VP-HP activation. In a pocket scratch, activation of FT-KE occurs during HR-KF activation. In a caudal scratch, activation of FT-KE occurs after the cessation of HR-KF activation. The timing characteristics of these muscle activity patterns correspond to the timing characteristics of changes in the angles of the knee joint and the hip joint obtained with movement analyses (21). We recorded electroneurographic (ENG) potentials from peripheral nerves of the hindlimb during each of the three forms of the “fictive” scratch in the spinal turtle immobilized with neuromuscular blockade (see Fig. 4). Common to all forms of the fictive scratch is the rhythmic alternation of the activity of hip protractor motor neurons (VP-HP) and hip retractor motor neurons (HR-KF). Each form displays a characteristic timing of the activity of knee extensor motor neurons (FT-KE) with respect to the cycle of VP-HP and HR-KF motor neuron activity. The timing characteristics of these motor neuron activity patterns are similar to the timing characteristics of the muscle activity patterns obtained in the preparation with movement (cf. Figs. 1 and 4). The motor pattern for each scratch form is generated centrally within the spinal cord. In the spinal immobilized preparation, neuromuscular blockade prevents both limb movement and phasic sensory input, and complete spinal transection isolates the cord from supraspinal input.(ABSTRACT TRUNCATED AT 400 WORDS)


2018 ◽  
Author(s):  
Rebecca Vaadia ◽  
Wenze Li ◽  
Venkatakaushik Voleti ◽  
Aditi Singhania ◽  
Elizabeth M.C. Hillman ◽  
...  

SummaryProprioceptors provide feedback about body position that is essential for coordinated movement. Proprioceptive sensing of the position of rigid joints has been described in detail in several systems, however it is not known how animals with an elastic skeleton encode their body positions. Understanding how diverse larval body positions are dynamically encoded requires knowledge of proprioceptor activity patterns in vivo during natural movement. Here we applied high-speed volumetric SCAPE microscopy to simultaneously track the position, physical deformation, and temporal patterns of intracellular calcium activity of multidendritic proprioceptors in crawling Drosophila larvae. During the periodic segment contraction and relaxation that occurs during crawling, proprioceptors with diverse morphologies showed sequential onset of activity throughout each periodic episode. A majority of these proprioceptors showed activity during segment contraction with one neuron type activated by segment extension. Different timing of activity of contraction-sensing proprioceptors was related to distinct dendrite terminal targeting, providing a continuum of position encoding during all phases of crawling. These dynamics could endow different proprioceptors with specific roles in monitoring the progression of contraction waves, as well as body shape during other behaviors. We provide activity measurements during exploration as one example. Our results provide powerful new insights into the body-wide neuronal dynamics of the proprioceptive system in crawling Drosophila, and demonstrate the utility of our approach for characterization of neural encoding throughout the nervous system of a freely behaving animal.


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