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Lungfish axial muscle function and the vertebrate water to land transition.

Horner AM, Jayne BC - PLoS ONE (2014)

Bottom Line: The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates.The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics.Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, California State University, San Bernardino, California, United States of America.

ABSTRACT
The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates. The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics. Lungfish are an ideal group to study the role of axial function in terrestrial locomotion as they are the sister taxon to tetrapods and regularly move on land. Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty. We compared terrestrial lungfish data to data from lungfish swimming in different viscosities as well as to salamander locomotion. The terrestrial locomotion of lungfish involved substantial activity in the trunk muscles but almost no tail activity. Unlike other elongate vertebrates, lungfish moved on land with a standing wave pattern of axial muscle activity that closely resembled the pattern observed in terrestrially locomoting salamanders. The similarity in axial motor pattern in salamanders and lungfish suggests that some aspects of neuromuscular control for the axial movements involved in terrestrial locomotion were present before derived appendicular structures.

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Representative EMGs from lungfish locomotion in different media.Motor patterns are compared among three conditions: fully terrestrial locomotion on mud (A), swimming in a very viscous solution (B), and in water (C; modified from [15]. Sites 1–5 (light shading) and 6–8 (dark shading) are from myomeres in the trunk and tail, respectively. EMGs during terrestrial locomotion were higher in amplitude, active for a greater proportion of a cycle, restricted mainly to the trunk region, and active almost simultaneously. Conversely, lungfish swimming is powered primarily by caudal muscle activity that is propagated posteriorly. For the sequence shown in panel A, the electrode at site 6 was dislodged.
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pone-0096516-g002: Representative EMGs from lungfish locomotion in different media.Motor patterns are compared among three conditions: fully terrestrial locomotion on mud (A), swimming in a very viscous solution (B), and in water (C; modified from [15]. Sites 1–5 (light shading) and 6–8 (dark shading) are from myomeres in the trunk and tail, respectively. EMGs during terrestrial locomotion were higher in amplitude, active for a greater proportion of a cycle, restricted mainly to the trunk region, and active almost simultaneously. Conversely, lungfish swimming is powered primarily by caudal muscle activity that is propagated posteriorly. For the sequence shown in panel A, the electrode at site 6 was dislodged.

Mentions: The EMGs of superficial ipsilateral sites in the trunk region during terrestrial locomotion were nearly synchronous, whereas swimming lungfish clearly had posteriorly propagated (traveling) waves of muscle activity (Figs 2–4). During terrestrial locomotion, EMGs from the most anterior (site 1) and most posterior (site 5) locations in the trunk region overlapped an average of 85.0±11.9% (Fig. 5). By contrast, ipsilateral EMGs in the trunk region of lungfish overlapped less than 10% for swimming, even in a very viscous solution (6.4±4.6%; Fig. 5). For all types of lungfish locomotion, none of the pairs of EMGs from opposite sides at the same longitudinal location had overlapping activity, and activity rhythmically alternated between the left and right sides as has been widely described for other vertebrates that move via lateral undulations.


Lungfish axial muscle function and the vertebrate water to land transition.

Horner AM, Jayne BC - PLoS ONE (2014)

Representative EMGs from lungfish locomotion in different media.Motor patterns are compared among three conditions: fully terrestrial locomotion on mud (A), swimming in a very viscous solution (B), and in water (C; modified from [15]. Sites 1–5 (light shading) and 6–8 (dark shading) are from myomeres in the trunk and tail, respectively. EMGs during terrestrial locomotion were higher in amplitude, active for a greater proportion of a cycle, restricted mainly to the trunk region, and active almost simultaneously. Conversely, lungfish swimming is powered primarily by caudal muscle activity that is propagated posteriorly. For the sequence shown in panel A, the electrode at site 6 was dislodged.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4008594&req=5

pone-0096516-g002: Representative EMGs from lungfish locomotion in different media.Motor patterns are compared among three conditions: fully terrestrial locomotion on mud (A), swimming in a very viscous solution (B), and in water (C; modified from [15]. Sites 1–5 (light shading) and 6–8 (dark shading) are from myomeres in the trunk and tail, respectively. EMGs during terrestrial locomotion were higher in amplitude, active for a greater proportion of a cycle, restricted mainly to the trunk region, and active almost simultaneously. Conversely, lungfish swimming is powered primarily by caudal muscle activity that is propagated posteriorly. For the sequence shown in panel A, the electrode at site 6 was dislodged.
Mentions: The EMGs of superficial ipsilateral sites in the trunk region during terrestrial locomotion were nearly synchronous, whereas swimming lungfish clearly had posteriorly propagated (traveling) waves of muscle activity (Figs 2–4). During terrestrial locomotion, EMGs from the most anterior (site 1) and most posterior (site 5) locations in the trunk region overlapped an average of 85.0±11.9% (Fig. 5). By contrast, ipsilateral EMGs in the trunk region of lungfish overlapped less than 10% for swimming, even in a very viscous solution (6.4±4.6%; Fig. 5). For all types of lungfish locomotion, none of the pairs of EMGs from opposite sides at the same longitudinal location had overlapping activity, and activity rhythmically alternated between the left and right sides as has been widely described for other vertebrates that move via lateral undulations.

Bottom Line: The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates.The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics.Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, California State University, San Bernardino, California, United States of America.

ABSTRACT
The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates. The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics. Lungfish are an ideal group to study the role of axial function in terrestrial locomotion as they are the sister taxon to tetrapods and regularly move on land. Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty. We compared terrestrial lungfish data to data from lungfish swimming in different viscosities as well as to salamander locomotion. The terrestrial locomotion of lungfish involved substantial activity in the trunk muscles but almost no tail activity. Unlike other elongate vertebrates, lungfish moved on land with a standing wave pattern of axial muscle activity that closely resembled the pattern observed in terrestrially locomoting salamanders. The similarity in axial motor pattern in salamanders and lungfish suggests that some aspects of neuromuscular control for the axial movements involved in terrestrial locomotion were present before derived appendicular structures.

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