A three-dimensional kinematic analysis of tongue flicking in Python molurus
1 Section Evolutionary Morphology, Institute of Biology (IBL), Leiden
University, PO Box 9516, 2300 RA Leiden, The Netherlands
2 Experimental Zoology Group, Wageningen Institute of Animal Sciences
(WIAS), Wageningen University, Marijkeweg 40, 6709 PG, Wageningen, The
Netherlands
* Author for correspondence (e-mail: j.h.de_groot{at}lumc.nl)
Accepted 3 December 2003
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Summary |
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Key words: snake, tongue, tongue sheet, muscular hydrostat, flicking, curvature, 3-D kinematics, high-speed fluoroscopy, X-ray
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Introduction |
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The mechanisms of tongue protrusion and superimposed tongue flicking in
snakes are still poorly understood. The intrinsic and extrinsic muscles
involved were identified by morphological studies
(Gnanamuthu, 1937;
Hershkowitz, 1941
;
Frazzetta, 1966
;
Langebartel, 1968
;
Kier and Smith, 1985
;
Smith and Mackay, 1990
),
electromyographical recordings (Meredith
and Burghardt, 1978
; Smith,
1984
,
1986
;
Herrel et al. 1998
) and
kinematic observations (Smith,
1984
,
1986
;
Bels et al. 1994
;
Herrel et al. 1998
). In
contrast to several other squamate taxa, snake tongues lack hard skeletal
support. Instead, the tongue behaves like an almost incompressible muscular
hydrostat (cf. Kier and Smith,
1985
) with interesting similarities to the highly extensible
muscular tentacles in squid (van Leeuwen
and Kier, 1997
). Muscle fibre activation leads to complex
distributions of fibre forces and fluid pressures that `drive' the
deformations in the tongue. A quantitative analysis of the tongue is
challenging due to complex connective tissue and muscle fibre arrangements,
highly non-linear mechanical tissue properties and very large
deformations.
The protruding tongue must satisfy three important mechanical demands.
First, a negative longitudinal pressure gradient is required in the tongue,
similar to that in an extending squid tentacle
(Van Leeuwen and Kier, 1997);
second, a sufficiently high axial stiffness to prevent excessive bending;
third, enough longitudinal compliance to accommodate the extreme overall
elongation of
100% (Smith,
1984
). Superimposed tongue flicking requires precisely controlled
spatial variations in axial compliance and bending moments.
To understand the mechanical contribution of the tongue muscles in terms of
forces and work, and consequently tongue architecture, a number of steps is
proposed (as summarised by Van Leeuwen et
al., 2000) that include (1) the measurement of the architecture
and tissue properties, (2) the development of a quantitative model that
predicts the optimal design of the system and (3) the acquisition of
experimental data for comparison with model predictions. A spatial
forward-dynamics model of snake tongue is currently being developed
(Van Leeuwen, 2002
) that
accepts microscopic data on tongue morphology
(Smith and Mackay, 1990
) and
material properties of the tissues as input.
In the present paper, we quantify the forward translation and internal
elongation of the whole tongue body, i.e. from the proximal tongue ensheathing
to the point of bifurcation (Fig.
1), and distinguish between the contribution of the posterior
portion of the tongue and the anterior (extended) portion of the tongue. We
quantify the mechanical behaviour of the tongue during flicking, in particular
its protrusion and spatial kinematics. The selected kinematic variables such
as local tongue acceleration, velocity and position and the changing 3-D shape
of the tongue are similar to those derived from forward dynamic simulations
(e.g. Chiel et al., 1992;
Van Leeuwen and Kier, 1997
;
Van Leeuwen, 2002
).
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We applied two techniques to record the tongue kinematics of the Burmese
python (Python molurus bivittatus). The deformation of the whole
tongue was recorded by high-speed fluoroscopy
(Snelderwaard et al.,
2002). The 3-D kinematics of the protruded and flicking tongue
that extends out of the mouth was obtained by high-speed photogrammetry
developed for the recording of spatial soft-tissue deformation
(de Groot and Van Leeuwen,
2002
). First, a general description of the tongue morphology and
muscle function is presented to facilitate understanding of the experimental
procedures, kinematic analysis and functional interpretation.
Tongue morphology
The snake tongue, schematically represented in
Fig. 1A, can be divided into
three portions: (1) the distal bifurcated tongue tips, (2) an anterior portion
of the tongue, which protrudes out of the mouth during tongue flicking, and
(3) a posterior portion of the tongue that remains almost entirely within the
mouth during protrusion (Smith and Mackay,
1990). The tongue is suspended in the floor of the mouth by a
folded tongue sheet that is dorsally stiffened by the larynx and trachea
(McDowell, 1972
). The origin
of the tongue sheet attaches at the posterior end of the tongue body and
inserts at the transition between the anterior and the posterior portions of
the tongue (Fig. 2A). In the
fully retracted tongue, the `outer sheet' covers the complete tongue
(Fig. 2B). Anteriorly, the
sheet folds inward and forms a second `inner sheet'. The inner sheet covers
the anterior portion of the retracted tongue. When the tongue is fully
extended, the sheathing is completely unfolded and envelops only the outer
surface of the posterior portion of the tongue
(Fig. 2C;
McDowell, 1972
; J. H. de Groot
and I. van der Sluijs, personal observations). Only the outer sheet is
connected to the floor of the mouth and allows the posterior portion of the
tongue to elongate freely, without straining the connective tissues of the
mouth floor.
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The major tongue muscles, the paired m. hyoglossus, originate from the
posterior part of the external tongue skeleton, i.e. the cartilaginous hyoids.
The individual muscles converge in a V shape, `enter' the tongue and extend
along the entire length of the tongue while keeping their separate identity
(Hershkovitz, 1941; Langebartel,
1968; McDowell,
1972
; Smith and Mackay,
1990
). The mm. hyoglossi continue into the tongue tips. Activation
of the extrinsic posterior portion of the mm. hyoglossi generates retracting
forces on the whole tongue body. Activation of the intrinsic mm. hyoglossi
tends to shorten the tongue locally due to the longitudinal arrangement of the
muscle fibres. Spatial leftright asymmetry of the intrinsic
longitudinal muscle fibre activation results in lateral bending forces.
The antagonists of the extrinsic part of the mm. hyoglossi are the mm.
genioglossi, originating from the dentary bone and inserting into the
posterior part of the outer sheathing
(Frazzetta, 1966;
Langebartel, 1968
;
McDowell, 1972
). Activated mm.
genioglossi generate protracting translation forces on the tongue base,
preventing the tongue base of the elongating tongue from moving posteriorly
(cf. chameleon tongue projection; Herrel
et al., 2000
; de Groot and Van
Leeuwen, in press
) and contributing to the forward tongue
translation.
The muscle fibre distribution in the anterior portion of the tongue differs
from the posterior portion (Hershkowitz,
1941; Kier and Smith,
1985
; Smith and Mackay,
1990
). A transverse section of the posterior portion of the tongue
reveals the paired longitudinal mm. hyoglossi, the transversal m. verticalis
and m. transversus and the circumferential m. circularis
(Kier and Smith, 1985
;
Smith and Mackay, 1990
). In
the anterior portion also, dorsal longitudinal bundles are found (Hershkovitz,
1941; Smith and Mackay, 1990
).
Contraction of the circumferential and transverse muscles results in a tongue
diameter decrease and, due to the incompressible character of the muscular
hydrostat, tongue elongation (Kier and
Smith, 1985
; Chiel et al.,
1992
). The combined antagonist contraction of the longitudinal
muscle fibres of the mm. hyoglossi and dorsal longitudinal muscles results in
the shortening of the tongue body. Dorso-ventral bending of the anterior
tongue depends on the contractile state of the mm. hyoglossi and the dorsal
longitudinal muscles, in combination with gravitational forces
(Smith and Kier, 1989
).
Electromyographical (EMG) recordings in snakes
(Meredith and Burghardt, 1978)
and other tongue-flicking squamates
(Smith, 1984
;
Herrel et al., 1998
) indicated
an involvement of the mm. genioglossi during protraction and the mm. hyoglossi
during subsequent retraction. Activation of intrinsic tongue muscle fibres was
recorded in combination with tongue kinematics (mm. hyoglossi, m. circularis)
during tongue protrusion of Tupinambis and Varanus during
feeding. Intrinsic longitudinal straining of more than 100% coincided with the
activity of m. circularis (Smith,
1984
,
1986
).
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Materials and methods |
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In the following, the tongue is defined as the non-bifurcated portion of the tongue body. The motions of the tongue tips were not quantified.
High-speed fluoroscopy
Surgically inserted radio-opaque (lead) markers helped to identify the
positions of relevant landmarks of the tongue. High-speed X-ray fluoroscopy of
these markers allowed us to measure the separate contributions of whole tongue
translation and length changes of the tongue to protrusion and retraction. The
python was instrumented under complete anaesthesia (200 ml
min1 of 1.5% isofluoran, 135 ml min1
N2O). The chosen marker locations
(Fig. 1B) were based on careful
dissections of preserved and freshly frozen specimens of Python molurus
bivittatus and related species (Python sebae, Python regius and
Boa constrictor constrictor). The markers were either glued on or
injected into different structures of the tongue system. The glued markers
were disk-shaped (height0.2 mm,
The instrumented python was placed into a plastic (Plexiglas) tunnel (1
mx0.3 mx0.3 m) that could be moved relative to the X-ray camera
system. Lateral images of the tongue at 250 frames s1
(shutter 1/3000 s) were stored by recording the X-ray fluoroscopy image of the
internal image intensifier with a high-speed digital camera (Kodak Motion
Analyzer SR-500, resolution 512x480 pixels;
Snelderwaard et al., 2002).
Only tongue flick sequences with long tongue lengths and performed in the
mid-sagittal plane of the head (within approximately 15°) were selected
for analysis, thus minimising 2-D projection artefacts due to lateral curving
of the tongue. Selection was instantly made through visual inspection. After
each successful recording, a perforated metal plate was recorded in the plane
of the tongue flick. The grid image was used to calibrate the image (scaling
and correction of image deformation) by means of a custom-made computer
programme. Finally, nine recordings were selected, and the positions of all
markers were digitised. The positions of markers 610 were expressed in
the head-fixed coordinate frame using markers 15. The position
(x) of the radio-opaque markers and their mutual longitudinal
distances (l) were determined in two tongue positions: the initial
position at rest (x0, l0) and at
maximum tongue protrusion with the tongue straight in front of the mouth
(xm, lm). Subsequently, the tongue
translation relative to the head,
d=(xmx0), and maximum
tongue strain,
max=(lml0)/l0,
were calculated.
3-D motion analysis
The python was placed in a plastic tunnel of 1.0 mx0.3 mx0.3 m.
At one end of the tunnel, a `collar' of three mirrors was placed with an
opening that just fitted the head of the python. The angle of the mirrors with
the vertical frontal plane was 45°. A high-speed digital camera
(Kodak Motion Analyzer SR-500, resolution 512x480 pixels) was placed at
1 m in front of the opening.
The python was lured to put her head through the opening with rat scent on
cotton wool. Once through the hole, the head and the exposed tongue were
projected by the three mirrors (Fig.
3). In each camera frame, four images of the head and tongue were
obtained: frontal (A), right lateral (B), dorsal (C) and left lateral (D),
resulting in four synchronous projections of the 3-D position of the tongue
relative to the head. The parameters that relate the image coordinates to 3-D
positions were calibrated by direct linear transformation (DLT; see
Woltring and Huiskes, 1990).
This resulted in 11 DLT parameters per image that were valid for all
subsequent frames of a tongue-flick event due to the fixed positions of camera
and mirrors.
Three tongue-flick sequences were recorded at 250 frames
s1. Assuming symmetry along the central axis of the tongue,
the 3-D position of the central axis of the tongue could be derived from the
contours of the tongue projections. The method used here was described in
detail elsewhere (de Groot and Van Leeuwen,
2002).
For each recorded frame, the coordinates of the finite 3-D tongue axis,
i.e. from mouth opening to the point of bifurcation, were described by a
third-order polynomial curve. This curve was defined by a coefficient vector
P=(a0, a1,
a2, a3, b0,
b1, b2, b3,
c0, c1, c2,
c3) and variable s. For each value of
0s
1 and for the given P-coefficients, a unique
combination of x, y and z coordinates was defined (e.g.
Van der Helm et al., 1992
):
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Each of the four images recorded in one frame was calibrated by means of 11 DLT parameters and resulted in a unique mathematical relationship between the 2-D projections and the 3-D coordinates. Thus, for each combination of 2-D image coordinates (u, v), a spatial 3-D position (x, y, z) could be calculated and vice versa. The position of the tongue axis was estimated by calculating the single combination of P-coefficients for which the projection of the 3-D tongue axis [x(s), y(s), z(s)] optimally fitted the recorded and digitised projections of the central tongue axis (u, v) in each of the four images in the frame. This optimal fit was obtained by application of a simplex optimisation routine. This procedure was repeated for each recorded frame. Thus, for each frame of the recorded tongue-flick sequence, a set of 12 P-coefficients was obtained. For n frames, the result is a time trace of nx12 coefficients. Finally, the time trace of each coefficient was filtered (25 Hz low-pass recursive Butterworth filter), which resulted in a mathematical 3-D description of the tongue axis for a complete tongue flick.
The P-coefficients (and thus the local x, y and z coordinates of the central tongue axis) were calculated in the coordinate system of the calibration frame. The coordinates were subsequently expressed in the local coordinate system of the snake head with the x-axis as the longitudinal axis of the mid-sagittal plane, i.e. from caudal to rostral, the y-axis as the vertical axis of the mid-sagittal plane, i.e. from ventral to dorsal, and the z-axis as the right lateral axis, i.e. from medial to the right-hand side.
From the 3-D description, we derived the external protrusion length by integration along the longitudinal axis for each recorded image from the mouth opening to the bifurcation point of the tongue. Protrusion velocity and acceleration were obtained from the first and second time differential of the external length trace. Tongue curvature, C (= 1/radius), along the axis was numerically determined from 51 points along the tongue axis for s=(0, 0.02,..., 1) (equations 1, 2, 3). A circle with radius r and centre M was numerically calculated for each set of three contiguous points along the tongue axis (Fig. 4).
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The 3-D time trace or trajectory of the bifurcation point of the tongue during the flick was obtained from equations 1, 2, 3 for s=1. The velocity and acceleration in the three coordinate directions were obtained from the first and second time differential of the position of the bifurcation point.
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Results |
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The tongue positions and translations relative to the `fixed' marker at the
mouth floor (marker 6; Fig. 1)
and lengths and deformations are summarised in
Table 1. The initial position
of the tongue in the mouth varied with a standard deviation (S.D.)
of 16.6 mm. The initial tongue length (25 mm) was almost constant
(S.D.=0.54 mm). The maximum tongue length showed a large variation,
as reflected by the high S.D. The general variation will even be
higher as we made a selection of tongue flick clusters based on direction and
sufficient length. The forward tongue translation, i.e. the average
displacement of markers 9 and 10 in the mm. hyoglossi, was 5.3±0.99 mm.
This translation is controlled by external muscle forces and was denoted as
the whole tongue translation. The posterior end of an elongating tongue would
tend to move caudally in the absence of such forces. The total tongue
protrusion was, on average, more than 110% of the initial tongue length:
10% originated from tongue translation and
100% from tongue
elongation. The elongation of the tongue was not uniformly distributed. The
mean longitudinal strain of the posterior portion of the tongue, defined by
post=
lpost/l0,post,
was 1.28, while the mean longitudinal strain of the anterior portion, defined
by
ant=
lant/l0,ant,
was 0.60.
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Three-dimensional high-speed photogrammetry
The 3-D motion of the longitudinal tongue axis was derived for three
tongue-flick clusters. The 3-D analysis was necessarily restricted to the
externally visible protruded portion of the tongue. The duration of a flick
cluster, defined from the moment that the tongue tips appeared to the moment
that they disappeared, was 0.60 s for the first cluster of three flicks, 0.46
s for the second cluster and 0.42 s for the third cluster. The tongue tips
made a remarkable `clapping' motion at the early appearance of the tongue. The
two tongue tips were slightly apart initially. Subsequently, the tips adducted
maximally, abducted and adducted again prior to the appearance of the point of
bifurcation. After this double `clapping' motion, the tongue tips finally
abducted and separated for the full duration of the flicking cluster. The
motion of the bifurcated tongue tips was not further included in the
quantitative 3-D analysis.
The 3-D description of the tongue position allowed the analysis of the kinematics along the longitudinal axis of the tongue, i.e. tongue length, protrusion velocity and protrusion acceleration (Table 2), and the 3-D kinematics of the tongue in the global coordinate system, i.e. the trajectory, velocity and acceleration of the bifurcation point and tongue curvature (Tables 2, 3). The maximum external tongue length ranged between 16 mm and 20 mm. The maximum protrusion velocity was observed at the moment of appearance of the tongue body (Fig. 5) and ranged between 0.31 m s1 and 0.43 m s1. The maximum tongue length was reached at the first downward flick in each of the three flick clusters (Fig. 5). The tongue tips in the first and second cluster touched the ground during this initial flick.
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The trajectory and kinematics of the bifurcation point were derived from
equations 1,
2,
3 for s=1, and the 3-D
shape of the tongue was determined every 4 ms for 0s
1. The
tongue axis was visualised from three mutually perpendicular viewpoints, e.g.
lateral, frontal and dorso-ventral (Fig.
6). The velocity and acceleration of the bifurcation point is
shown in Fig. 7 and summarised
in Table 3. The velocities and
accelerations in the vertical y-direction were slightly higher than
those in the horizontal x-direction. The selected tongue flicks
remained close to the sagittal plane and resulted therefore in relatively low
lateral velocities (±0.1 m s1) and accelerations
(±5 m s2) in the z-direction. The time trace
of the covered distance of the bifurcation point is assumed equivalent to the
spatial exposure of the tongue, i.e. the amount of sampled air during the
flicks (Fig. 8). The recorded
traces show more or less the same slope for the three flicking sequences with
a mean velocity of the bifurcation point of 0.25 m s1 within
a range of 0.04 m s1 to 0.65 m s1. The
covered distance of the bifurcation point was almost proportional to the total
duration of the tongue flick. The maximum covered distance for each of the
three flick sequences was 113 mm, 69 mm and 81 mm, respectively.
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The tongue curvature, C, averaged along the tongue and for each of
the flick clusters, was 0.06 mm1, with a maximum
curvature of
0.5 mm1
(Table 2). At the transition
between the tongue and the tongue tips, however, the maximum curvature ranged
from 1.5 mm1 to 2.0 mm1 during the final
upward stroke. The tips made an angle with the more posterior tongue body of
80°.
The motions of the tongue tips were not quantified. Here, we summarise some qualitative observations. During early protrusion, the tongue tips made a repetitive abduction and adduction, or double `clapping' movement, before separating. We could not discriminate whether this movement was a mechanical instability caused by the accelerating tongue or an intentionally controlled movement. During tongue flicking, the tongue tips moved relatively independently from the tongue and, in two flick sequences, the tongue tips touched the floor at the first downward oscillation (Figs 5, 6).
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Discussion |
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The mean resultant velocity vector, i.e. the average slope of the
cumulative covered distance in Fig.
8, was 0.25 m s1 for the three tongue flick
clusters analysed. The spatial and temporal exposure of the tongue seemed to
be more or less linearly correlated for the observed flicks. The temporal
exposure is a good predictor for the spatial exposure for these observed
tongue flicks, i.e. three independent approaches, provoked by the same
stimulus. For behavioural studies on a single specimen, the time of tongue
exposure may turn out to be an easy to record parameter for spatial exposure.
However, three tongue-flick clusters recorded from one specimen of python
during an explorative type of behaviour are not sufficient for a definite
conclusion.
The duration of tongue exposure, determined by Gove
(1979) for 26 ophidian
species, was minimally 100 ms with a mean duration of
150 ms. Tongue
exposure should be above a lower time limit, such that enough chemical
particles are collected for an adequate sensory transmission. The duration
will also be related to tongue length and flicking velocity (spatial exposure)
and the sensory capacity of the vomeronasal organ. With the present 3-D
recording technique we illustrate that it is now possible to quantify and
combine these spatial and temporal requirements.
Morphological and functional differentiation of the tongue
On the basis of observed morphological differences between the anterior and
posterior portion of the tongue, Smith and Kier
(1989) and Smith and Mackay
(1990
) proposed a functional
differentiation in the tongue body. The design of the posterior portion of the
tongue indicated an important contribution in tongue protrusion, while the
asymmetrical arrangement of the longitudinal fibres in the anterior portion
indicated an important role in flicking. Our high-speed fluoroscopic analysis
of the tongue protrusion revealed 10% forward translation of the tongue and,
simultaneously, 100% elongation of the whole tongue. The longitudinal strain
in the tongue was nonuniformly distributed. The posterior portion elongated
128% while the anterior portion elongated only 60%.
The tongue strains observed in Python and the strains reported in
Tupinambis (Smith,
1984) are of the same order of magnitude. The gross tongue
morphology of Python and Tupinambis also show
correspondence. The proposed mechanism of hydrostatic elongation of tentacles
and tongues (Kier and Smith,
1985
; Smith and Kier,
1989
) and illustrated by quantitative model simulations
(Chiel et al., 1992
;
van Leeuwen and Kier, 1997
) is
likely to be at work in the tongue of the Python. Elongation of the
tongue is realised by a decrease of the cross-sectional area of the tongue,
induced by shortening of the transverse, vertical and circumferential muscle
fibres in the tongue.
The exact role of the individual intrinsic muscle fibres during tongue
flicking in the entire tongue and specifically in the anterior tongue portion
is difficult to predict from our kinematic study. The gravitational and
inertial components, in combination with the muscle forces, resulted in the
observed tongue oscillations. Both concave and convex curvatures in the
sagittal plane were simultaneously observed along the tongue axis
(Fig. 9). During the tongue
flicks, curvature waves travelled along the tongue in both forward and
backward directions, indicated by the positive and negative slopes of the
green (curved) and red (linear) areas in
Fig. 9. The time traces of the
oscillations of the bifurcation point were not symmetrical (Figs
6,
7). The local stiffness of the
tongue along its axis is probably not constant but continuously adjusted by
muscular activity. The exact nature of this control and the mechanical
consequences cannot be derived from kinematics alone and need to be analysed
by dynamic model simulations (e.g. van
Leeuwen, 2002).
At the transition of the tongue to the bifurcated tongue tips, extreme curvatures of 1.52 mm1 were observed during the final upward motion of the bifurcation point in each of the three flick clusters (Fig. 9). Hydrostatic shortening requires a reduced tension in the circular muscles during retraction and, simultaneously, an increased tension in the retractors, which results in a lower bending stiffness of the tongue. The reduction of the length of the flicking tongue results in the redistribution of kinetic energy over a smaller tongue mass. The reduced vertical diameter of the tongue at the transition of the tongue body to the tongue tips in combination with the lower hydrostatic bending stiffness and the increase of kinetic energy may explain the extreme curvature during the final upward motion of the tongue tip.
The mechanism of tongue protrusion
In the Introduction, three demands on tongue protrusion were defined. For
the optimal forward protrusion, (1) a negative forward pressure gradient was
required in the muscular hydrostat; (2) sufficiently high stiffness was
required to control bending amplitude and (3) enough longitudinal compliance
was required to accommodate tongue protrusion. During protrusion, we observed
a forward translation of the tongue that must have originated from the mm.
genioglossi. The muscle compensated for the backward forces from the intrinsic
tongue elongation and generated positive work. Electromyogram (EMG) activity
of this muscle has indeed been demonstrated for tongue protrusion in snakes
(Meredith and Burghardt, 1978)
and other tongue-flicking squamates
(Smith, 1984
;
Herrel et al., 1998
).
The observed 130% elongation of the posterior portion of the tongue and the 10% superimposed forward translation leave no other conclusion but that a negative forward pressure gradient must have been generated in the muscular hydrostat. The negative forward pressure gradient is likely to be generated by the activation of m. transversus, m. verticalis and m. circularis and the simultaneous activation of the mm. genioglossi.
The second and third demand on the protruding hydrostat involved axial
stiffness in combination with longitudinal compliance. In the snake tongue,
the posterior portion of the tongue ejects the anterior portion of the tongue
and the tongue tips. In mechanical terms, the posterior soft body pushes the
anterior tongue mass out of the mouth. This function requires sufficient axial
stiffness to prevent buckling of the posterior tongue portion in combination
with longitudinal compliance. In most squamates, these requirements are solved
by the presence of an interior lingual process. Such stiff intrinsic
structures are absent in snake tongues
(Gnanamuthu, 1937;
Langebartel, 1968
), and a
solution must be contained in the actively controlled soft tissue.
Two solutions may increase the axial stability of a muscular hydrostat:
firstly, the incorporation of longitudinal muscle fibres in the
circumferential periphery of the tongue and, secondly, adding extrinsic
support from neighbouring tissues. Both solutions seem to be present in the
tongue. Dorsal longitudinal fibre bundles are present in the anterior portion
of the tongue (Hershkovitz, 1941; Smith
and Mackay, 1990). A combined activation of the longitudinal
muscle fibres (dorsal fibre bundles and intrinsic mm. hyoglossi) with the
transversal antagonists (m. transversus, m. verticalis and m. circularis)
results in a higher stiffness of the anterior tongue portion. The increased
longitudinal forces may explain the reduced strain of the anterior portion,
relative to the posterior portion of the tongue.
In the posterior portion of the tongue, such longitudinal muscle fibres in the circumferential periphery are absent, while a high axial stiffness is required in this portion because of the acceleration of the anterior tongue mass during protrusion. Intrinsic axial stiffness of the posterior portion of the tongue by means of peripheral longitudinal muscle fibres potentially reduces the protrusion forces and, consequently, the forward acceleration of the tongue mass. This is in conflict with the demand on longitudinal compliance. We propose that the tongue sheet and adjacent tissue substitute, at least partly, for the function of an internal stiff entoglossal process. External support of the protruding tongue mass prevents buckling and simultaneously enables longitudinal compliance.
The outer sheet is fixed in the mouth floor and is stiffened by the trachea
(McDowell, 1972) and envelopes
the posterior portion of the tongue (Figs
1,
2). Contraction of the muscles
in the mouth floor, e.g. the m. ceratomandibularis and the m.
intermandibularis (Frazzetta,
1966
; Langebartel,
1968
; McDowell,
1972
), increase the stiffness of the tongue sheet and, thus, the
external environment of the posterior tongue portion. The folded structure of
the sheet contributes to the longitudinal compliance of the posterior portion
of the tongue. Only the outer sheathing is connected to the mouth floor. The
inward fold inserts about halfway along the contracted tongue at the so-called
distal sheathing (Figs 1,
2). Elongation of the posterior
portion of the tongue results in the outward folding of the inner sheathing at
the distal fold (Fig. 2). Thus,
the folded structure functions as a lubricated lining for tongue protrusion
and subsequent retraction. Adventitiously, the tongue sheet is fully unfolded
at the maximum protrusion length (Fig.
2) and the stressstrain characteristics of the connective
tissue will constrain further tongue elongation.
The external solution for axial stiffness of the posterior portion of the
tongue is advantageous over the intrinsic solution in the anterior tongue
portion because it reduces the longitudinal contracting forces and the
effective tongue mass. This advantage is illustrated by the observed
differences in posterior and anterior strains. The anterior outer portion is
unsupported, i.e. the external stabilisation cannot be applied after
protrusion out of the mouth. Sagittal asymmetry of the longitudinal muscle
fibres is required to resist gravitational forces, and peripheral longitudinal
muscle fibres are needed for intrinsic stiffness against buckling and not the
least for flicking. Quite interestingly, the muscular tentacular stalks in the
squid Loligo pealei are mechanically supported by two of the eight
arms in the initial rapid extension phase during prey capture
(Kier and Van Leeuwen, 1997).
Perhaps, not surprisingly for a very similar combination of functional demands
(i.e. pushing and extreme elongation), extrinsic support also evolved here as
the solution to prevent buckling.
Experimental support for the proposed mechanism of tongue protrusion
We assumed axial stability in the posterior portion of the tongue in
combination with high compliance in the longitudinal direction as an important
demand for tongue protrusion. This demand is supported by observations in each
of the three analysed tongue flick clusters. (1) The highest accelerations are
generated while the tongue is still within the mouth and supported by the
tongue sheet: maximum tongue tip velocities were observed at the moment of
initial tongue tip protrusion out of the mouth
(Fig. 5). (2) The tongue tips
make a double `clapping' movement while leaving the mouth, which may indicate
mechanical instability during the initial acceleration. (3) After the tongue
body protrudes beyond the labia of the mouth, the protrusion velocity
decreases (Fig. 5) and the
unsupported tongue portion is not further accelerated. (4) The first tongue
flick coincides with the maximum tongue length, after which an overall
negative protrusion velocity is observed (Figs
5,
6). The negative acceleration
results in a dynamic stability of the tongue.
The mechanism of tongue retraction
Tongue retraction may be regarded as the opposite of tongue protrusion with
one major difference: during retraction, the tongue mass is pulled at instead
of pushed. Retraction of the tongue mass inherently provides dynamic
stability. The extrinsic part of the paired mm. hyoglossi is the only
candidate muscle to retract the whole tongue mass, and the intrinsic part of
the mm. hyoglossi to contract the tongue body (negative strain), anteriorly
assisted by the longitudinal dorsal muscles as previously suggested and
supported by EMG observations of the mm. hyoglossi of garter snakes
(Meredith and Burghardt, 1978)
and other tongue-flicking squamates
(Smith, 1984
;
Herrel et al., 1998
).
Reflection on the evolution of snake tongues
The reduction of the lingual process is supposed to be related to tongue
translations in chemoreception (Bels et
al., 1994) and coincides with the development of a tongue sheet in
the anguimorpha and snakes (McDowell,
1972
). Based on the importance of axial stability of the tongue
during protrusion, we hypothesised about the stability function of the
entoglossal process in squamates and the substitute role of the tongue sheet
for the absence of an internal skeletal support in snakes.
Stability of the unsupported tongue may well be a primary demand in the
squamate tongue, e.g. while drinking. This intrinsic stability requires the
development of peripheral longitudinal muscle fibres in the anterior portion
of the tongue. Modification of the peripheral muscle fibres subsequently
enabled tongue flicking. This development is supported by flicking
observations (Gove, 1979;
Herrel et al., 1998
) and
coincides with morphological transformations in the anterior tongue portion
(Smith and Mackay, 1990
).
Several authors used the tongue to study the taxonomic relationship between
snakes and (tongue-flicking) lizards. The classification was based on
morphological (McDowell, 1972)
and behavioural characters combined with kinematics
(Gove, 1979
), the
specialisation of the tongue towards chemoreception (e.g.
Bels et al., 1994
;
Kardong et al., 1997
) and
morphological characters combined with kinematics
(Smith and Mackay, 1990
;
Herrel et al., 1998
). We
cannot contribute to this discussion with our limited number of
observations.
However, the externally observed tongue flicking is the result of
`behavioural' constraints on spatial and temporal tongue exposure,
biomechanical interactions of constrained muscle dynamics and tongue inertia,
and `evolutionary' constraints in the inherited morphological and neurological
characters. These characters are therefore dependent and should be analysed in
an integrated manner. One means to study combined morphological characters and
physiological constraints is the forward dynamic model simulation (e.g.
Van Leeuwen, 2002). The
predicted kinematics should agree with the quantitative findings presented
here. The simulations will give insight into the mechanics and control of
tongue flicking and will give supplementary support for the present plausible
hypotheses on tongue protrusion and tongue flicking. By comparing predicted
optimal solutions with actual solutions found in nature, a better
understanding can be gained of the causal factors in the evolution of the
tongue.
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Acknowledgments |
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References |
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