Slow-tonic muscle fibers and their potential innervation in the turtle,Pseudemys (Trachemys)scripta elegans

Abstract

A description is provided of the ratio of slow-tonic vs. slow- and fast-twitch fibers for five muscles in the adult turtle, Pseudemys (Trachemys) scripta elegans. The cross-sectional area of each fiber type and an estimation of the relative (weighted) cross-sectional area occupied by the different fiber types are also provided. Two hindlimb muscles (flexor digitorum longus, FDL; external gastrocnemius, EG) were selected on the basis of their suitability for future motor-unit studies. Three neck muscles (the fourth head of testo-cervicis, TeC4; the fourth head of retrahens capitus collique, RCCQ4; transversalis cervicis, TrC) were chosen for their progressively decreasing oxidative capacity. Serial sections were stained for myosin adenosine triphosphatase (ATPase), NADH-diaphorase, and alpha-glycerophosphate dehydrogenase (alpha-GPDH). Conventional fiber-type classification was then performed using indirect markers for contraction speed and oxidative (aerobic) vs. glycolytic (anaerobic) metabolism: i.e., slow oxidative (SO, including slow-twitch and possibly slow-tonic fibers), fast-twitch, oxidative-glycolytic (FOG), and fast-twitch glycolytic (Fg) fibers. Slow-tonic fibers in the SO class were then revealed by directing the monoclonal antibody, ALD-58 (raised against the slow-tonic fiber myosin heavy chain of chicken anterior latissimus dorsi), to additional muscle cross sections. All five of the tested muscles contained the four fiber types, with the ATPase-stained fibers including both slow-tonic and slow-twitch fibers. The extreme distributions of SO fibers were in the predominately glycolytic TrC vs. the predominately oxidative TeC4 muscle (TrC-SO, 9%; FOG, 20%; Fg, 71% vs. TeC4-SO, 58%: FOG, 16%; Fg, 25%). Across the five muscles, the relative prevalence of slow-tonic fibers (4-47%) paralleled that of the SO fibers (9-58%). TeC4 had the highest prevalence of slow-tonic fibers (47%). The test muscles exhibited varying degrees of regional concentration of each fiber type, with the distribution of slow-tonic fibers paralleling that of the SO fibers. In the five test muscles, fiber cross-sectional area was usually ranked Fg > FOG > SO, and slow-twitch always > slow-tonic. In terms of weighted cross-sectional area, which provides a coarse-grain measure of each fiber type's potential contribution to whole muscle force, all five muscles exhibited a higher Fg and lower SO contribution to cross-sectional area than suggested by their corresponding fiber-type prevalence. This was also the case for the slow-twitch vs. slow-tonic fibers. We conclude that slow-tonic fibers are widespread in turtle muscle. The weighted cross-sectional area evidence suggested, however, that their contribution to force generation is minor except in highly oxidative muscles, with a special functional role, like TeC4. There is discussion of: 1) the relationship between the present results and previous work on homologous neck and hindlimb muscles in other nonmammalian species, and 2) the potential motoneuronal innervation of slow-tonic fibers ...

Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata)

“…Western blot analysis shows positive results for MAb 2F4c for the masticatory myosin isoform and ALD-58 for slow/tonic myosin isoforms, which suggests a more homogeneous fibre type within the jaw muscle in comparison to the thigh muscle based on the fibres we tested ( figure 3 c , d ). The MAb 2F4c is known to react with masticatory myosin while ALD-58 has been used in chicken and turtle experiments to identify tonic muscle fibres [ 23 ]. The presence of the masticatory myosin isoform was not surprising, as it is found widely in jaw muscles in mammalian systems [ 40 ].…”

“…Tonic fibres have unique contractile properties and do not contract with a twitch, but rather exhibit a prolonged, fatigue-resistant contraction that is similar to that of mammalian smooth muscle [22]. Slow-twitch and slow-tonic fibres both have been found in turtle hindlimb and neck muscles, and the two types have been identified as distinct from one another [23]. The primary role of tonic fibres is to facilitate fatigue-resistant behaviours involving stabilization and maintenance of postures in a variety of vertebrates [23][24][25][26][27], though they also may be involved in very slow locomotor performance as observed in chameleons [28] (but see [29]).…”

Electrophoretic separation of reptilian skeletal and cardiac muscle myosin heavy chain isoforms: Dependence on gel format

“…The studied turtle species (all native to Ohio) were the red‐eared slider ( Trachemys scripta elegans , Wied‐Neuwied 1839), common snapping turtle ( Chelydra serpentine , Linnaeus 1758), spiny softshell turtle ( Apalone spinifera , Lesueur 1827), painted turtle ( Chrysemys picta , Schneider 1783), and Common map turtle ( Graptemys geographica , Le Sueur 1817). The identification and nomenclature of turtle muscles were based on earlier reports . Fresh muscle samples were also obtained from a euthanized adult male water monitor ( Varanus salvator , Laurenti 1768) and adult female prehensile tailed skink ( Corucia zebrata ; Gray 1856).…”

The myosin light chain 1 isoform associated with masticatory myosin heavy chain in mammals and reptiles is embryonic/atrial MLC1

“…The coracohyoideus was selected as a jaw-opener in turtles (Lemell et al, 2000). The flexor digitorum longus, with ~50% of the fibers reported to be slow, and the fourth head of the testocervicis, with many slow tonic fibers (Callister et al, 2005), were studied in each turtle species, as well. The iliofibularis, with predominantly fast fibers (Callister et al, 2005), was also sampled in the red-eared slider.…”