Activation patterns of the tongue-projector muscle during feeding in the imperial cave salamanderHydromantes imperialis

Abstract

Salamanders of the genus Hydromantes project their tongues the greatest distance of any amphibian to capture prey, up to 80% of body length or approximately 6·cm in an adult individual. During tongue projection on distant prey, the tongue is shot ballistically and the tongue skeleton leaves the body of the salamander entirely. We investigated an aspect of the motor control of this remarkable behavior by examining electromyographic patterns within different regions of the tongue-projector muscle, the subarcualis rectus (SAR). SAR activation is strongly modulated, and features of this modulation can be predicted by tongue-projection distance (i.e. prey distance). The strap-like buccal portion of the SAR is always activated first and for the longest duration, compared to any other region. It is in a position to transmit force generated by the posterior SAR to the floor of the mouth, where it originates. The posterior SAR encompasses and applies force to the epibranchial of the tongue skeleton, and its activation pattern gradually changes from a posterior-to-anterior wave of activation onset during short-distance projection to an all-at-once pattern during the most extreme long-distance (ballistic) projection. The duration of activity and EMG area of each recorded region of the SAR increase with increasing prey distance, showing greater muscle recruitment during longdistance projection. No effect of prey-capture success was observed in the EMG patterns, indicating that SAR activation is controlled in a feed-forward manner.

Thermal effects on the performance, motor control, and muscle dynamics of ballistic feeding in the salamanderEurycea guttolineata

“…The activation patterns of the SAR in E. guttolineata accord with a pattern of muscle activation prior to tongue projection found in previous studies of other plethodontid species (Deban and Dicke, 2004;Deban et al, 2007) (Table 1 , Fig. 4, Fig.…”

“…1) (Deban et al, 1997;Deban and Dicke, 1999;Deban and Dicke, 2004;Deban et al, 2007;Deban and Richardson, 2011). Tongue-projection performance values overlapped with those previously measured for Eurycea over a much narrower range of temperatures (22-24°C) (Deban et al, 2007).…”

“…A similar mechanism has been found in jumping frogs, in which both muscle shortening and elastic recoil occur during launch (Roberts and Marsh, 2003;Astley and Roberts, 2012). The activation of muscles well in advance of high-powered movements is a common phenomenon, having been found or implicated not only in salamanders (Deban and Dicke, 2004;Deban et al, 2007) but also in other high-powered movements in both vertebrates and invertebrates (Wainwright and Bennett, 1992a;Wainwright and Bennett, 1992b;de Groot and van Leeuwen, 2004;Patek et al, 2004;Burrows, 2006;Patek et al, 2006;Van Wassenbergh et al, 2008;Patek et al, 2007;Burrows, 2009;Anderson and Deban, 2010;Deban and Lappin, 2011;Roberts and Azizi, 2011;Anderson and Deban, 2012;Sandusky and Deban, 2012;Anderson and Higham, 2014;Higham and Anderson, 2014).…”

“…Electromyographic (EMG) recordings of muscle activity during feeding in plethodontid salamanders with ballistic tongue projection (Hydromantes and Bolitoglossa) have shown that, on the brief timescale of tongue projection, the SAR becomes active well before the tongue leaves the mouth (Deban and Dicke, 1999;Deban and Dicke, 2004;Deban et al, 2007), and this activity nearly ceases by the onset of tongue projection (Deban et al, 2007). This pattern indicates a phase in which the SAR myofibers contract and load collagenous elements of the muscle with potential energy that is subsequently released to power tongue launch.…”

Dynamics and thermal sensitivity of ballistic and non-ballistic feeding in salamanders

“…Each tongue projector muscle surrounds one of the paired, elongated, tapered epibranchial cartilages that extend caudally from the buccal region. Each epibranchial connects rostrally to paired ceratobranchials, which in turn articulate rostrally with the medial, unpaired basibranchial that lies in the floor of the mouth and supports the sticky tongue pad (Lombard and Wake, 1977;Wake and Deban, 2000;Deban, 2002;Deban and Dicke, 2004). In elastically powered, ballistic tongue projection, activation of the SAR muscles 80-200 ms prior to tongue launch stretches collagenous tissues within the muscles.…”