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First published online January 31, 2007
Journal of Experimental Biology 210, 655-667 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02664
Extremely high-power tongue projection in plethodontid salamanders
1 Department of Biology, 4202 East Fowler Avenue, SCA 110, University of
South Florida, Tampa, FL 33620, USA
2 Department of Organismal Biology and Anatomy, University of Chicago, 1027
E. 57th Street, Chicago, IL 60637, USA
3 Brain Research Institute, University of Bremen, 28334 Bremen,
Germany
4 Experimental Zoology Group, Wageningen Institute of Animal Sciences
(WIAS), Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The
Netherlands
* Author for correspondence (e-mail: sdeban{at}cas.usf.edu)
Accepted 22 November 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: elastic storage, amphibian, feeding, inverse dynamics, kinematics, muscle
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Olson and Marsh, 1998;
Alexander, 2002).
In musculoskeletal systems that are capable of rapid movements, the power
that is required to produce the observed velocity and acceleration often
exceeds the peak instantaneous power output capability of vertebrate muscle,
which has been measured at 1121 W kg–1 (in quail pectoralis)
(Askew and Marsh, 2001). In
systems that have power requirements in excess of what muscle can produce
directly, muscles are still performing the work required for the movement.
However, the rate of performing the work is decoupled from the rate at which
it is transmitted to the environment. This decoupling typically results in
greater rates of energy release (i.e. higher power) and relies on the presence
of elastic structures, such as tendons and aponeuroses, which lie between the
muscle and the point of interaction with the environment. These structures are
deformed by muscle forces and subsequently recoil to perform the same work
much more quickly than the muscle
(Alexander, 2002).
One such ballistic system in which `elastic power enhancement' has been
implicated is jumping in the bushbaby Galago senegalensis. The vastus
muscle complex of these mammals generates up to 2350 W kg–1
(Bennet-Clark, 1976), and is
hypothesized to store energy in aponeuroses, energy that is released during
the latter part of the push-off (Aerts,
1998). Another ballistic system that is particularly relevant to
the current study is tongue projection in the chameleon, in which the required
muscle-mass-specific power output reaches 3168 W kg–1. It is
thought that this power output is achieved by the deformation and recoil of
nested collagenous sheaths within the tongue muscle
(de Groot and van Leeuwen,
2004).
Like chameleons, some plethodontid salamanders are capable of ballistic
tongue projection over great distances; the tongue can be projected up to 80%
of body length in less than 20 ms. The distance of tongue projection, combined
with the short duration over which projection occurs, suggests that tongue
projection is a high-power behavior, and that elastic power enhancement may
occur (Deban et al., 1997;
Deban and Dicke, 1999;
Deban and Dicke, 2004).
Using a combination of kinematic analyses, inverse dynamics and electromyographic recordings from the tongue projector muscles, we investigated the mechanics of tongue projection in representatives of each the three clades of plethodontid salamanders that have independently evolved ballistic tongue projection. Goals of this study were to (1) determine the work and power output of ballistic tongue projection in each of the three clades with ballistic projection; (2) determine if sufficient muscle is available, in each clade, to directly produce the observed power, or if an elastic power enhancement system must be operating; and (3) determine whether the timing of projector muscle activity relative to tongue movements is consistent with direct muscle action or with the alternative mechanism of elastic power enhancement.
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Materials and methods |
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Salamanders were imaged at 22–24°C in lateral or dorsal view while feeding on crickets, termites, waxworms and flour beetles. Images were obtained from one individual each of Hydromantes platycephalus (62 mm snout–vent length, SVL) and H. imperialis (70 mm SVL), two individuals of H. genei (63 and 67 mm SVL), seven individuals of Bolitoglossa dofleini (70–125 mm SVL), one Eurycea guttolineata (49 mm SVL) and two Eurycea wilderae (30 and 32 mm SVL). The cave salamanders (H. imperialis and H. genei) fed more readily in low light, hence they were imaged at 1000, 1600 or 2000 Hz with a Redlake MotionPro (Tucson, AZ, USA) using a single fiber optic microscope lamp 1 m from the subject combined with a retro-reflective background to yield a sharp silhouette of the salamander (Fig. 1). The H. platycephalus were recorded with a NAC (Simi Valley, CA, USA) HCS1000 and the Bolitoglossa and Eurycea were recorded using a Redlake MotionMeter, all at 1000 Hz with synchronized stroboscopic illumination, yielding greyscale video images of the salamanders (Figs 2, 3). A calibration grid of 1 cm squares was imaged separately, in the same plane as the animal, for each set of trials to eliminate parallax problems.
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Kinematic analysis
The x,y coordinates of the tongue tip were recorded for each frame
of the video sequences (using NIH Image running on a Macintosh computer),
starting with the first appearance of the tongue at the mouth and ending with
the withdrawal of the tongue pad into the mouth at the end of tongue
retraction (see supplementary material, Movies 1–3). Maximum tongue
reach was calculated as the maximum excursion of the tongue tip (i.e. rostral
tip of tongue skeleton) from its initial position. Relative maximum tongue
reach was expressed as a percentage of SVL.
The movement of the tongue tip was used in the dynamics calculations
because the tongue tip was visible throughout projection, and because it was
deemed an acceptable surrogate for the movement of the center of mass of the
projected tongue. Two sources of error could arise from using the tongue tip
as a surrogate for center of mass, both involving potential shifting of the
center of mass relative to the tongue tip: caudal shifting of the tongue pad
on the tongue skeleton during tongue acceleration, and folding of the tongue
skeleton. We examined preserved specimens of all genera and compared them to
the feeding images and conclude that these sources of error are slight. The
tongue pad changes length by no more than 6% during the period of maximum
acceleration (in the 21 feeding sequences in which it was measured in
Hydromantes, Eurycea and Bolitoglossa), and the tongue
skeleton is folded (i.e. ceratobranchial, epibranchial and basibranchial are
nearly collinear) when the tongue tip reaches the distance from the mouth at
which maximum acceleration is achieved [a thorough discussion of tongue
skeleton folding is published elsewhere
(Lombard and Wake, 1976;
Lombard and Wake, 1977)].
Instantaneous velocity, acceleration and mass-specific power of the
projected tongue were calculated from the position data. A quintic spline was
fitted to the raw position data using QuickSAND
(Walker, 1997), because this
technique is unlikely to overestimate velocities and accelerations
(Walker, 1998). The
interpolation function was used and the program yielded smoothed position,
velocity and acceleration values at a final rate of 5000 Hz, regardless of the
rate of the original data (1000–2000 Hz). The smoothing parameter, P,
for the quintic spline was adjusted separately for each feeding trial so that
secondary oscillations were removed from the acceleration trace. This required
greater smoothing than necessary to remove these oscillations from the
position and velocity data, and resulted in more conservative estimates of
acceleration and velocity. Instantaneous mass-specific power of the tongue was
calculated by multiplying the instantaneous velocity by the corresponding
instantaneous acceleration.
The observed tongue-mass-specific power was then converted to required muscle-mass-specific power (i.e. the specific power that the muscles must produce to explain the observed kinematics). The masses of the tongue and the paired tongue projector muscles (left and right sides summed) were measured in preserved and fresh specimens of Hydromantes imperialis, Bolitoglossa dofleini and Eurycea guttolineata. Tongue mass included the combined mass of the tongue skeleton, the tongue pad, and a portion of the retractor muscle (m. rectus cervicis) equal to the length of the tongue skeleton. Preserved tongues were rehydrated in amphibians Ringer solution prior to weighing. Muscle-mass-specific power output values that would be required by the projector muscles (required specific power) were computed by multiplying the observed specific power values of the projected tongue by the average ratio of tongue mass to projector muscle mass (T/M ratio), which was 0.79 for Bolitoglossa, 1.04 for Hydromantes, and 1.29 for Eurycea.
Mass-specific work of the projector muscles (J kg–1) was calculated by taking the area under the positive portion of the mass-specific power–time curve. The required mass-specific power and mass-specific work values for the muscles computed are underestimates, not only because of smoothing of the position data but also because the frictional forces and other drag forces that resist tongue projection are assumed to be zero in this analysis. In the animal, some energy is expended to overcome these forces.
Times of maximum tongue reach, maximum velocity, maximum acceleration and maximum power were calculated with respect to the time (t=0) at which tongue instantaneous power reached 1% of the maximum value for that feeding event.
Electromyography of the projector muscle
Electromyographic (EMG) recordings and high-speed video recordings were
made from one of the bilaterally paired tongue projector muscles (m.
subarcualis rectus, SAR) in three individuals of Bolitoglossa
dofleini while they fed on crickets.
The morphology of the feeding system of plethodontid salamanders and the
EMG methods used here are discussed in a previous paper
(Deban and Dicke, 2004) and
are reviewed here only briefly. During tongue projection, the elongated tongue
skeleton folds medially, becoming a compact projectile as it is pulled and
squeezed forward relative to the ceratohyals by the paired SAR muscles. The
posterior portion of the SAR (SARP) encompasses the elongated epibranchial
cartilages and is in series with the anterior portion (SARA) that inserts on
the ceratohyal cartilages in the floor of the mouth. In the species examined
here, the tongue skeleton is free from the SAR muscles and can be projected
completely from the mouth in a ballistic fashion. It is attached to the body
of the salamander by a bundle of tissue that includes the retractor muscles
(i.e. the rectus cervicis, RC), blood vessels, nerves and a connective tissue
sheath. After the tongue is fully projected, it is withdrawn into the body by
the RC muscles, which originate on the pelvis and insert into the tongue pad.
These lengthy muscles are slack and even pleated when the tongue is at rest in
the mouth (Lombard and Wake,
1977; Deban et al.,
1997).
Electrodes were implanted through three or four small incisions in the skin, at the surface of the muscles. An electrode was placed against the anterior portion of the SAR in two individuals through an incision in the skin of the throat.
Formvar-coated nichrome wire was used to construct bipolar patch
electrodes. Prior to electrode implantation, salamanders were anesthetized by
immersion in a buffered 2% aqueous solution of MS-222 (3-aminobenzoic acid
ethyl ester; Sigma, St Louis, MO, USA) for 10–30 min. Electrodes were
implanted through a small incision in the skin onto the surface of the right
SAR muscle midway along its length. Electrode leads were glued together with
modeling glue and attached to the skin of the back with suture. The ends of
the leads were soldered to metal connectors, which were plugged into the probe
of the amplifier (Deban and Dicke,
1999).
Salamanders fed readily after recovery from anesthesia, which typically
took less than 30 min. Recordings were made within 3 days of recovery, after
which electrode positions and spacing were confirmed surgically. A total of 25
feedings from three individuals were recorded. Electromyographic signals were
amplified 2000 times by a Grass P511 (West Warwick, RI, USA) differential
amplifier. Signals were recorded at a rate of 2000 samples
s–1 on an Apple (Cupertino, CA, USA) Macintosh PowerPC G3
using a National Instruments (Austin, TX, USA) PCI-6034E analog-to-digital
card and a custom LabVIEW program. The raw signals were rectified and filtered
in LabVIEW to remove 60 Hz line noise, other noise, and low-frequency movement
artifacts (Deban and Dicke,
2004).
EMG and video recordings of feedings were made while salamanders stood in a thin layer of water connected to ground in a transparent plastic box, with the retro-reflective material beneath the box. Live crickets were dropped on the substrate in front of the salamander to induce feeding. The trigger output on the video camera was connected to a separate channel on the data acquisition card, allowing synchronization of the EMG signals and the videos to within one video frame (1–2 ms).
Analysis of electromyograms
Five measurements were made from the rectified EMG burst associated with
each prey-capture strike: (1) time of the onset of activity, the time after
which activity exceeded background noise levels by twofold for at least 10 ms;
(2) time of the offset of activity, the time after which activity dropped
below two times background noise levels for at least 10 ms; (3) burst area,
the area under the rectified EMG burst (in units of mV s) between times 1 and
2; (4) duration of activity, the onset time minus the offset time, and (5)
peak amplitude, the rectified EMG area (in units of mV s) of the 10 ms period
of the burst in which this value was maximal.
For each prey-capture strike, the SAR activation-projection delay was calculated by subtracting the SAR EMG onset time (1 above) from the time of the first appearance of the tongue at the mouth (taken from the synchronized video sequence).
The SAR activation–projection delay corresponds roughly to the duration of time that is available for any elastic structures that are in series with contractile elements to be loaded with potential energy. This loading period was used to estimate the average muscle-mass-specific power that would have to be generated by the projector muscles for each feeding attempt, the average muscle-mass-specific power input, by taking the average muscle-mass-specific power output and multiplying it by the ratio of unloading period duration (i.e. time to maximum velocity) to loading period duration. The loading duration includes the unknown time required after activation for the projector muscle to develop tension (i.e. the `electromechanical delay').
To examine the relationship between projector muscle activation and tongue projection kinematics, four analyses of covariance (ANCOVAs) were performed with individual as the effect and one of four EMG variables as the covariate: SAR activation–projection delay, SAR EMG burst duration, SAR EMG burst area, and SAR EMG peak amplitude. The ANCOVAs examined the effects of individual and each of these four EMG variables on nine kinematic variables: maximum velocity, maximum tongue reach, maximum acceleration, maximum muscle-mass-specific power, muscle-mass-specific work, time of maximum tongue reach, time of maximum velocity, time of maximum acceleration and time of maximum power output. The inclusion of an individual term in the model accounted for the influence of individual variation, both biological variation and electrode variation. Individual variation was present in a few variables, but will not be discussed. The individual x covariate interaction was not significant for any variable in any of the four analyses, so it was dropped from the model to improve statistical power. These analyses were performed using StatView 5.0 for Macintosh.
Least-squares regressions and coefficients of determination (r2) were calculated for variables that showed a significant effect in the ANCOVAs, to examine the relationship between EMG and kinematic variables.
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Results |
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Duration of tongue protraction (i.e. time to maximum tongue reach) was less than 20 ms in all feedings of all species, and the greatest in Hydromantes (8–19 ms), followed by Bolitoglossa (3–13 ms) and Eurycea (4–11 ms) (Table 1).
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Tongue projection kinematics
Maximum velocities and accelerations of the tongue during projection were
high, in accordance with the brief duration of the movement
(Table 1). Average maximum
velocities were highest in Hydromantes genei (4.6±0.1 m
s–1, maximum 4.9 m s–1, means ±
s.e.m.), followed by H. imperialis (4.0± 0.0 m
s–1, maximum 4.2 m s–1),
Bolitoglossa (3.8±0.1 m s–1, maximum 7.0 m
s–1), H. platycephalus (2.7±0.2 m
s–1, maximum 3.7 m s–1), Eurycea
wilderae (2.5±0.1 m s–1, maximum 3.1 m
s–1) and E. guttolineata (2.3±0.2 m
s–1, maximum 2.7 m s–1).
Average maximum accelerations were highest in Bolitoglossa (1740±109 m s–2, maximum 4492 m s–2), followed by Eurycea wilderae (1377±104 m s–2, maximum 1992 m s–2), H. genei (1009±58 m s–2, maximum 1174 m s–2), H. imperialis (810±108 m s–2, maximum 918 m s–2), E. guttolineata (792±64 m s–2, maximum 1039 m s–2) and H. platycephalus (413±65 m s–2, maximum 984 m s–2).
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Total muscle-mass-specific work performed during tongue projection ranged from 0.9 to 19.5 J kg–1, averaging 6.3±1.2 J kg–1. H. genei performed the most average muscle-mass-specific work at 11.2 J kg–1 and E. guttolineata the lowest at 3.7 J kg–1 (Table 1).
Projector muscle activation
The EMG recordings from Bolitoglossa dofleini reveal that the SAR
muscle (i.e. tongue projector muscle) began activity 0.082–0.213 s
before the tongue leaves the mouth. This SAR activation–projection delay
averages 0.117±0.005 s (mean ± s.e.m.)
(Fig. 5). SAR EMG burst
duration averages 0.171±0.012 s (from 0.073 to 0.282 s), burst area
averages 12.4±0.7 mV s (from 5.1 to 20.2 mV s), and peak amplitude
averages 0.71±0.04 mV (from 0.271 to 1.144 mV).
The average power estimated to have been generated by the SAR during the 0.117 s loading period (the average muscle-mass-specific power input) ranged from 10 to 167 W kg–1 and averaged 54±4 W kg–1.
Both SAR activation–projection delay and SAR EMG area had a significant, positive, effect on maximum tongue reach, maximum tongue velocity, and total muscle-mass-specific work, as shown by the ANCOVA (Table 2). SAR activation–projection delay additionally had a significant, positive effect on the time of maximum velocity and the time of maximum power output. There was no significant effect of EMG duration or EMG peak amplitude on any of the kinematic variables. Maximum muscle-mass-specific power output was not significantly affected by any of the EMG variables. SAR activation–projection delay showed a coefficient of determination (r2) of 0.22 with maximum tongue reach, 0.26 with maximum tongue velocity, 0.24 with total muscle-mass-specific work, 0.22 with time of maximum velocity, and 0.21 with time of maximum power output (Fig. 6). SAR EMG area has an r2 of 0.21 with maximum tongue reach, 0.22 with total muscle-mass-specific work, and 0.24 with maximum velocity (Fig. 7).
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Discussion |
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;
Deban and Dicke, 1999;
Deban and Dicke, 2004). The
Bolitoglossa and Eurycea displayed tongue projection of
shorter duration than Hydromantes; however, these species did not
project their tongues to as great distance as Hydromantes, in neither
absolute nor relative terms. This results are in accord with predictions based
on the morphology of the tongue apparatus, namely that the length of the
folded tongue skeleton (particularly the epibranchials) is greatest in
Hydromantes (Lombard and Wake,
1976; Lombard and Wake,
1977).
The duration of tongue projection in all these species is very brief when
compared to published values from other salamander taxa. The brief tongue
projection durations are no doubt related to the ballistic mode of tongue
projection, in which high velocities must be achieved to propel the tongue to
the target under its own momentum. Among other salamanders in the family
Plethodontidae that lack ballistic projection, some take about the same time
to protract the tongue as Hydromantes (13±1 ms), but all take
longer than Eurycea and Bolitoglossa (both 7±0.04
ms): Ensatina eschscholtzii protracts the tongue fully in an average
of 15 ms (Deban, 1997a),
Pseudotriton ruber requires 11 ms
(Deban, 1997b), Plethodon
glutinosus takes 19 ms, and Desmognathus quadramaculatus takes
37 ms (Larsen, Jr et al.,
1989). Salamanders from other families, none of which have free
tongue pads or ballistic projection, require still longer: Ambystoma
mabeei takes 16 ms, A. cingulatum takes 87 ms
(Beneski, Jr et al., 1995),
Ambystoma tigrinum 40 ms (Dockx
and de Vree, 1986), Salamandra salamandra 22–84 ms
(Dockx and de Vree, 1986;
Miller and Larsen, Jr, 1990),
Paramesotriton hongkongensis 112 ms
(Miller and Larsen, 1990);
Taricha torosa 80–140 ms
(Findeis and Bemis, 1990),
Hynobius kimurae 25 ms and H. nebulosus 36 ms
(Larsen et al., 1996).
The distance of tongue protraction also varies widely among salamanders
(Wake and Deban, 2000).
Hydromantes, Eurycea and Bolitoglossa (and all other
bolitoglossines) possess enhanced tongue projection abilities, in both brevity
and reach. Their maximum tongue projection distances range from 31 to 64% of
SVL and 16 to 40 mm (Table
1). In comparison, Ambystoma californiense can protract
its tongue 2.4 mm beyond the jaw tips and A. mabeei only 0.3 mm
(Beneski, Jr et al., 1995);
Salamandrella keyserlingii protracts its tongue 6.6 mm
(Wake and Deban, 2000),
Tylototriton verrucosus 2.7 mm, and Salamandrina terdigitata
7.4 mm (Miller and Larsen, Jr,
1990). Relative tongue reach distances reported are 7% of SVL for
the plethodontids Desmognathus quadramaculatus and Plethodon
jordani, and 15% in Ensatina eschscholtzii
(Wake and Deban, 2000). Among
those taxa previously studied with ballistic tongue projection,
Bolitoglossa occidentalis projects its tongue up to 17 mm or 44% of
SVL (Thexton et al.,
1977; Larsen, Jr et al.,
1989), Bolitoglossa subpalmata has been recorded reaching
30 mm, and Hydromantes italicus 50 mm
(Roth, 1976), and the greatest
tongue reach occurs in Hydromantes supramontis, which has been
recorded projecting its tongue 60 mm or 80% of SVL
(Deban et al., 1997).
Maximum tongue projection velocities and accelerations have not been
published for other salamander species, but they have been measured in the
chameleon, another ballistic-tongued animal. Chameleo pardalis and
C. melleri produce peak accelerations of the tongue pad of
340–374 m s–2, and a peak velocity of 6 m
s–1 (de Groot and van
Leeuwen, 2004), and Chameleo oustaleti achieves a peak
acceleration of 490 m s–2
(Wainwright et al., 1991). The
velocity is higher than the highest velocity achieved by the salamanders (4.6
m s–1 in Hydromantes), but the chameleon's
accelerations are much lower (compared to 413–1740 m
s–2 in the salamanders). This makes sense when we consider
that the chameleons that have been studied are much larger animals, have a
longer `track' on which to accelerate the tongue to a given velocity, compared
to the salamanders, and shoot their tongues a greater absolute and relative
distance. A similar pattern emerges from the comparison of values among the
salamander species of this study. Hydromantes have the longest
epibranchials and projector muscles, by far, with which to accelerate the
tongue. Two of the Hydromantes have the lowest accelerations, two
have greater velocity, and all have greater tongue reach than the other
taxa.
The total mass-specific work performed by the salamander tongue projector
muscles (maxima are 5–20 J kg–1;
Table 1) is at the lower end of
the range of values obtained from other vertebrate musculoskeletal systems,
suggesting that the muscles may be working, on average, at low strain and/or
low stress. Work is estimated at 28 J kg–1 in
Chameleo [56 mJ 2 g–1
(de Groot and van Leeuwen,
2004)]. In the pectoralis muscles of various birds of different
sizes, work ranged from 16 to 56 J kg–1, with the larger
values achieved by the larger birds (Askew
et al., 2001). Limb muscles of jumping bullfrogs averaged 27 J
kg–1 (with a strain of 26% in one muscle)
(Olson and Marsh, 1998). In
mouse soleus muscles, work was measured at 4.5–15.5 J
kg–1 with in vitro work loop experiments with
strains ranging from 6–11% of resting muscle length (the highest work
corresponded to the highest strain) (Askew
and Marsh, 1997). One estimate of maximum work for skeletal muscle
is 57–113 J kg–1, given a maximum stress of
200–400 kPa (kN m–2) and a strain of 30%
(Pennycuick, 1992). However,
when work is computed as the area under the curve of isometric tension plotted
against length, values as high as 220 J kg–1 (for frog
striated muscle) are estimated (Alexander
and Bennet-Clark, 1977). If we assume that the tongue projector
muscles of salamanders are maximally recruited, the calculated work values
suggest that the muscles spend little or no time near the portion of their
length–tension curves where high stress is developed, or they operate at
low strains, or both.
Required muscle power output
Instantaneous required mass-specific power output of the tongue projector
muscle, the SAR, in the salamanders studied here is extremely high
(2443–18129 W kg–1) when compared to other muscular
systems that have been studied, both episodically and cyclically contracting
muscles. Among episodic systems, the semimembranosus muscle of Rana
pipiens, when used in maximal jumping, reached 373 W
kg–1, as shown by in vitro contractile experiments
(Lutz and Rome, 1996). The
jumping musculature in hylid frogs was estimated from kinematics of high-speed
movies to produce an average required muscle-mass-specific power of 500 W
kg–1 (Marsh and
John-Alder, 1994), and a peak instantaneous muscle-mass-specific
power that is probably twice that, 1000 W kg–1. An even
higher value was estimated for the hind limb muscles of the bushbaby,
Galago senegalensis, which achieved 2350 W kg–1
(Bennet-Clark, 1976), a figure
confirmed by in vivo inverse dynamics analysis
(Aerts, 1998). The tongue
projector muscle of the chameleon achieves 2340–3168 W
kg–1 for required muscle-mass-specific power output
(de Groot and van Leeuwen,
2004), and the jaw depressor muscles of the toad Bufo
achieve the highest value yet, 9600 W kg–1 during ballistic
mouth opening (Lappin et al.,
2006).
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),
mouse extensor digitorum longus muscles achieve 372 W kg–1 in
in vitro maximum isotonic power
(Askew and Marsh, 1997), and
the iliofibularis muscles of the lizard Dipsosaurus dorsalis which
are used in acceleration, achieved 460 W kg–1 at 40°C,
measured in vitro (Marsh and
Bennett, 1985). Based on the breaking strength of the muscle
tendons, the pectoralis of the pigeon is estimated at 860 W
kg–1 maximum (Pennycuick
and Parker, 1966), and based on in vitro work loop
experiments, that of the quail achieves 1121 W kg–1
(Askew and Marsh, 2001). A
similar value was estimated for accelerating lizards of the genus
Acanthodactylus: 952 W kg–1 in vitro and
940 W kg–1 in vivo
(Curtin et al., 2005).
In any musculoskeletal system in which connective tissue is in series with
a muscle, the work of the muscle is redistributed temporally to some extent
due to compliance of the connective tissue
(Alexander, 2002). In certain
cases, this redistribution can result in very high rates of energy release
(i.e. power output) because some tissues, such as collagen, are stiffly
elastic and can store strain energy and then release that energy faster than
the contractile elements of muscle. Maximizing power output is critical for
performance of ballistic movements such as throwing, tongue projection and
jumping, because these movements require high kinetic energy to be achieved
within a limited excursion (Alexander,
1968; Olson and Marsh,
1998; Alexander,
2002). Although a small amount of elastic strain energy can be
stored in muscle tissue (Alexander and
Bennet-Clark, 1977), in many systems with power enhancement, such
as jumping in frogs, fleas and locusts, and punching in stomatopods, the
energy is stored in connective tissues outside the muscle tissue
(Bennet-Clark and Lucey, 1967;
Bennet-Clark, 1975;
Peplowski and Marsh, 1997;
Olson and Marsh, 1998;
Patek et al., 2004).
Examples of the storage of strain energy that results in increased power
production in vertebrates include tongue projection in chameleons and toads,
jumping in bushbabies, and accelerating in turkeys. In the chameleon, the work
of the accelerator muscle of the tongue is redistributed temporally by elastic
structures in the tongue. This set of nested connective tissue sheaths
surrounds the tongue skeleton and strain longitudinally when the accelerator
muscle contracts. As they slide off the end of the tongue skeleton the sheaths
recoil radially and help to accelerate the tongue pad
(de Groot and van Leeuwen,
2004). In toads, elastic structures at both the origin and
insertion of the depressor mandibulae muscle as well as within the muscle
itself have been demonstrated to recoil during the fast mouth opening that
powers tongue projection (Lappin et al.,
2006). Elastic storage also occurs in the hindlimbs of
accelerating, running turkeys, which achieve peak muscle-mass-specific power
outputs over 400 W kg–1
(Roberts and Scales, 2002).
The system is thought to achieve this high-power output via a
mechanism in which tendons in series with extensor muscles store energy during
the first half of stance and then release energy and propel the bird during
the second half of stance. In the bushbaby, the aponeuroses within the vastus
muscle–tendon complex get stretched during the pre-jump crouch and
during the early part of push-off and recoil later in push-off, to increase
the power output of the vastus muscles
(Aerts, 1998).
In salamander tongue projection, no elastic, energy-storing structures have
been definitively identified, but two lines of evidence suggest that an
elastic power enhancer is operating: the high-power output calculated for
tongue projection that is discussed above, and the timing of projector muscle
activation relative to tongue movements. In Bolitoglossa the
projector muscle becomes active 82–213 ms (average 117±5 ms)
before the tongue appears at the mouth, which is sufficient time for elastic
structures to be loaded prior to recoil. The muscle fibers of the SARP are
short (
1 mm) and exclusively fast twitch
(Dicke et al., 1995) and, as
such, probably reach peak tension within 30 ms of the start of electrical
activity, as do other amphibian fast twitch muscles
(Luff and Proske, 1979;
Lännergren et al., 1982;
Lutz and Rome, 1996), and
could begin stretching series elastic elements well before that. Aponeuroses
lie in series with the muscle fibers in the complex SARP muscle
(Fig. 8) and a double-layered
collagenous sheath lines the lumen of the muscle, either of which may act as a
spring. However, it is not yet known how these structures are loaded during
muscle contraction. The SAR activation–projection delay is similar in
duration to that of the other ballistic feeding systems with power
enhancement: in Chameleo, the tongue accelerator muscle is activated
200–300 ms prior to the start of tongue projection
(Wainwright and Bennett, 1992;
de Groot and van Leeuwen,
2004), and in Bufo, EMG activity of the jaw depressor
muscles begins 150–250 ms prior to ballistic mouth opening
(Lappin et al., 2006).
Also in accord with the hypothesis of a power enhancer are the estimated
values of the maximum power that the SAR generates during the hypothesized
loading phase of tongue projection. These values (17–436 W
kg–1, average 129±11 W kg–1) are
within the physiological limits for direct power production of other skeletal
muscles that have been studied, which have maxima that range from
174–1121 W kg–1
(Marsh and Bennett, 1985;
Lutz and Rome, 1996;
Askew and Marsh, 1997;
Williamson et al., 2001;
Curtin et al., 2005). The
average value of 129 W kg–1 is comparable to that of
Chameleo, which is estimated at 144 W kg–1
(de Groot and van Leeuwen,
2004).
One last piece of evidence that supports the power enhancement model is the
relationship between SAR muscle activity and tongue projection kinematics.
When a muscle performs work there should be correlations between certain EMG
parameters and the amount of work performed. For example, in breathing in
alligators, the EMG activity of several ventilatory muscles is positively and
significantly correlated with tidal volume
(Farmer and Carrier, 2000). In
a system in which the muscle applies force through a series elastic element,
energy is still conserved and that relationship should persist. In
Hydromantes, SAR EMG area has been shown to be positively and
significantly correlated with maximum tongue reach
(Deban and Dicke, 2004). In
the Bolitoglossa examined here, SAR EMG area is positively and
significantly correlated with maximum tongue reach, maximum tongue velocity
and total muscle-mass-specific work, as expected
(Table 2). However, because
elastic elements should essentially uncouple the rate of work production by
the muscle (i.e. power input) from the rate of work performed on the tongue
skeleton (i.e. power output), which is measurable kinematically, we expect no
correlation between SAR EMG area and maximum power output. There is in fact no
relationship between SAR EMG area and maximum muscle-mass-specific power
output. The timing of muscle activation relative to tongue movements, on the
other hand, should show a relationship with kinematic performance measures,
because we expect that loading of elastic structures will take longer in
tongue projection episodes of greater effort. SAR activation–projection
delay is in fact positively and significantly correlated with several
performance measures including maximum tongue reach, maximum velocity, and
total muscle-mass-specific work (Table
2). Maximum power production is not correlated with any EMG
parameter measured, indicative of an uncoupling of power produced by the
muscle and power manifest in the projected tongue.
Conclusions
The available evidence points to an elastic power enhancer in the ballistic
tongue-projection mechanism of plethodontid salamanders, animals which achieve
tongue projection distances far greater than other salamanders and project the
tongue fully in far less time. This high-power system appears to have evolved
concomitantly with ballistic projection in the Plethodontidae, three times
independently. Such a system requires three components: a motor to generate
mechanical work (i.e. energy), a spring to store the energy, and a latch to
control the timing of unloading of the spring. The motor has been identified
as the paired subarcualis rectus muscles. What remains to be discovered are
the anatomical structures that make up the spring and the latch. In other
systems, collagen acts as the spring that stores energy and increases the
instantaneous power output of the muscular system, either in the form of
tubular sheaths as in the chameleon or aponeuroses as in the bushbaby. In the
SARP of Hydromantes (Fig.
8), collagen fibers lie in series with the short muscle fibers in
the form of aponeuroses as well as a double-layered sheath surrounding the
lumen (similar to the situation in chameleons), providing two viable
candidates for the spring. The morphology of the SARP of the other species
examined here is very similar to that of Hydromantes, and likely also
contain these collagenous structures. Future work will focus on determining
how these structures are loaded prior to tongue projection and how much energy
they can store. The latch remains to be identified, but we expect that it is
under muscular control to allow elastic elements to be loaded to varying
degrees before tongue projection commences, a hypothesis based on the
documented ability of these salamanders to precisely modulate their tongue
projection distance and velocity (Deban
and Dicke, 1999; Deban and
Dicke, 2004).
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Acknowledgments |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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