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First published online November 28, 2008
Journal of Experimental Biology 211, 3908-3914 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.021345
The functional significance of the lower temporal bar in Sphenodon punctatus
1 Laboratory of Functional Morphology, Department of Biology, University of
Antwerp, Universiteitsplein 1, B-2610 Antwerpen, Belgium
2 Department of Organismic and Evolutionary Biology, Harvard University, 26
Oxford Street, Cambridge, MA 02138, USA
3 Department of Organismal Biology and Anatomy, University of Chicago, Chicago,
IL 60637, USA
* Author for correspondence (e-mail: vicky.schaerlaeken{at}ua.ac.be)
Accepted 20 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: Sphenodon punctatus, lower temporal bar, feeding behavior, bite force, static bite model
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). In the
past, the loss of a contact between jugal and quadratojugal was interpreted as
unique for squamates and, therefore, many ancient diapsids (e.g.
Prolacerta, a Triassic archosaur; Paliguana, a Permian
reptile) were considered to be squamates
(Müller, 2003;
Wu, 2003). However, modern
cladistic analysis has shown that the absence or loss of the lower temporal
bar should be considered an ancestral trait for many diapsids
(Gauthier et al., 1988;
Müller, 2003).
Despite the importance of the lower temporal bar in debates regarding basal
amniote relationships, the functional significance of the presence or absence
thereof remains obscure. One often cited hypothesis suggests that reduction of
the lower temporal bar allowed for an increase in the volume of the external
jaw adductor leading to an increase in bite force
(Rieppel and Gronowski, 1981).
Yet, the loss of the lower temporal bar probably also affects the stability of
the jaw suspension, as reaction forces on the jaw during biting will induce
moments at the jaw and quadrato–squamosal joints that could be resisted
by a complete bar (Herrel et al.,
1998a).
The redevelopment of the lower temporal bar in animals such as S.
punctatus has been argued to stabilize the quadrate and allow precise
occlusion (Wu, 2003;
Lu et al., 2008), or to
facilitate the development of a propalineal power stroke
(Gorniak et al., 1982),
enabling these animals to break down relatively large or tough prey. However,
these advantages may have come at the cost of a reduction in bite force
capacity and feeding efficiency if indeed jaw adductors are constrained by the
presence of a lower temporal bar.
Lepidosaurians provide an excellent test case for these hypotheses as
S. punctatus, the only extant representative genus of the
Rhynchocephalia, has a complete lower temporal bar
(Fig. 1). Lizards, by contrast
(the closest extant relatives of S. punctatus), are characterized by
the lack of the lower temporal bar
(Rieppel and Gronowski, 1981)
(Fig. 1) and their feeding
mechanics are relatively well known (e.g.
Smith, 1982;
Smith, 1984;
Bels et al., 1994;
Herrel et al., 2001c;
Schwenk, 2000;
Bels, 2003). In the present
study, we explore the functional role of the lower temporal bar by comparing
data on morphology, bite force and feeding kinematics in S. punctatus
as well as in squamates with a generalized cranial morphology. We test whether
S. punctatus has: (1) less jaw adductor muscles, (2) lower bite
forces, and (3) needs more jaw cycles to process prey compared with lizards.
Additionally, we use a static bite model to explore whether the redevelopment
of a complete lower temporal bar in S. punctatus is a consequence of
the reorganization of the jaw adductors and/or the development of the musculus
pterygoideus atypicus (Wu,
2003) and may be associated with the presence of a unique shearing
bite.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). All jaw
muscle bundles of one side were removed and stored in 70% ethanol until
weighed at the Functional Morphology Laboratory at the University of Antwerp.
Muscles were blotted dry and weighed on a Mettler MT5 electronic balance
(accuracy, ±0.01 mg; Mettler-Toledo Inc., Columbus, OH, USA)
(Table 1).
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Next, muscles were transferred to a 30% aqueous nitric acid solution and
left for 20–24 h after which the solution was replaced by a 50% aqueous
glycerin solution. Individual fibers were teased apart using blunt-tipped
glass needles, and 10 fibers were selected randomly and drawn using a
binocular microscope with attached camera lucida (MT5 Wild, Wild Heerbrugg
Ltd., Heerbrugg, Switzerland). Drawings were scanned and fiber lengths
determined using Image TpsDig software
(Rohlf, 2001) (freeware
available at
http://life.bio.sunysb.edu/morph).
The mean fiber length per bundle was determined and the physiological
cross-section of each bundle was approximated by the ratio of the mass over
the mean fiber length, assuming a muscle density of 1000 kg
m–3 (Table
2).
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Animals and husbandry
Data on bite forces and feeding behavior for S. punctatus were
obtained from a series of juveniles maintained at the Otorohanga Kiwi house,
Otorohanga, New Zealand. The animals were housed in a large glass vivarium on
a 12 h:12 h light:dark cycle and were offered water and food ad
libitum. The environmental temperature varied from 20°C during the
daytime to 10°C at night.
Bite forces
An isometric Kistler force transducer (type 9203, Kistler, Wintherthur,
Switzerland) mounted on a purpose-built holder and connected to a Kistler
charge amplifier (type 5058A, Kistler) was used to measure bite forces (for
details, see Herrel et al.,
1999a; Herrel et al.,
2001a; Herrel et al.,
2001b). Measurements were repeated five times for each animal
(N=14). The maximal value recorded out of the five trials was
considered the maximal bite force for each animal. Data for S.
punctatus were compared with previously unpublished bite force data for a
wide array of agamid species (87 individuals belonging to nine different
species) collected using similar methods.
Feeding behavior
Data on feeding behavior for S. punctatus were collected for three
individuals. As previous recordings of jaw movements indicated that these were
slow (Gorniak et al., 1982),
feeding behavior was recorded at 25 Hz using a digital camcorder (Sony, Tokyo,
Japan). Video recordings were reviewed using Midas Player software (Redlake,
San Diego, CA, USA; v. 2.1.7), and only feeding sequences where animals
remained perpendicular to the camera, and in which all the phases of a
transport cycle (slow open, SO; fast open, FO; fast close, FC; slow
close/power stroke, SC/PS) were present, were used in further analysis. A
total of 26 feeding sequences ranging from 5 to 29 cycles were retained to
calculate the transport and swallowing stage duration, the number of transport
and swallowing cycles, the mean transport cycle duration and the mean
swallowing cycle duration while eating a mealworm. Two externally visible
landmarks, the anterior tip of the upper jaw and the anterior tip of the lower
jaw, were digitized on each frame for 120 transport cycles of the three
individuals using Didge (Image Digitizing Software v. 2.2.0; Alistair Cullum).
Based on the x-y coordinates from these markers gape
distance was calculated. Velocities and accelerations associated with the
changes in gape distance over time were calculated from the filtered
displacement data (using a zero phase shift, fourth-order low pass Butterworth
filter at 25 Hz; implemented by Sam Van Wassenbergh) by numerical
differentiation.
To delineate the kinematic phases of a transport or swallowing cycle, we
used the jaw acceleration data: the duration of the slow open phase was
defined as the time between the beginning of a transport or swallowing cycle
and the first pronounced acceleration peak during jaw opening, the fast open
phase was defined as the time between the first acceleration and the
deceleration peak, the fast close phase was defined as the time between the
peak deceleration and peak acceleration during jaw closing, and the slow close
phase was defined as the time from the peak acceleration during closing until
the end of the cycle (see Schaerlaeken et
al., 2007; Schaerlaeken et
al., 2008).
Static bite model
The analysis of biting in S. punctatus relied on the computation
of the static force equilibrium. The model used was a modified version of the
one applied by Cleuren and colleagues
(Cleuren et al., 1995). Muscle
forces were simply scaled to their physiological cross-section (250 kPa)
(Herzog, 1994). Bite forces
thus calculated are in remarkable correspondence with in vivo bite
forces in some groups (Herrel et al.,
2008), supporting the validity of this method. Muscle orientation
was defined by the 3D-coordinates of the centres of origin and insertion. This
spatial information was gathered from prepared skulls and our dissection.
Bilaterally symmetrical muscle activation patterns are assumed (see
Gorniak et al., 1982). As a
result, only sagittal components of the muscle forces must be considered
because transverse components will cancel each other out. Mean fiber lengths,
muscle masses and coordinates of origin and insertion of jaw muscles for one
additional S. punctatus individual (svl, 22.1 cm; cl, 5.68 cm) were
obtained from the paper by Gorniak and colleagues
(Gorniak et al., 1982).
For the simulations, three groups of muscles were considered: the
bi-articular muscles crossing both the jaw and the quadrato–squamosal
joint (or the equivalent junction in S. punctatus), and two groups of
mono-articular muscles, crossing either the jaw or the
quadrato–squamosal joint/junction. Calculation of the moment exerted by
all jaw closers about the quadrato–mandibular joint allowed the
determination of magnitudes of the food reaction forces at selected bite
points. This was done for a range of orientations of food reaction forces [set
to vary between –42 and –138 deg. with respect to the lower jaw
(see Herrel et al., 1998a)],
as the actual orientation of the food reaction force is often unpredictable
and may depend upon the shape, texture and position of the food item, as well
as the shape and position of the teeth. Biting points (=point of application
of the food reaction forces; one on the anterior-most dentary tooth and one on
the posterior-most dentary tooth) were selected on the basis of observational
studies of feeding in unrestrained animals. These observations also showed
small gape angles during forceful biting. To standardize the simulations and
allow a comparison with previously published data
(Herrel et al., 1998a;
Herrel et al., 1998b), a fixed
gape angle of 10 deg. was used in our simulations.
Each food reaction force also exerts a moment about the quadrato–squamosal joint/junction, which must be annulled to maintain the static equilibrium condition. The moment required to counteract the effect of the food reaction force at the quadrato–squamosal joint/junction was calculated and termed the `required' moment. Bi-articular muscles used for biting inherently also exert a moment about the quadrato–squamosal joint/junction. This moment was calculated and summed to the moment generated by mono-articular muscles when present. Premising a static quadrate, the difference between this moment and the required moment (i.e. remaining required moment) must therefore be induced by structures other than muscles (e.g. ligaments or bone as in S. punctatus). Joint forces are those forces acting from the jaw on the quadrate with the opposite sign and direction of the joint reaction forces. Conventionally, counter-clockwise moments in lizards facing to the right are regarded positive, clockwise moments as negative.
Statistical analyses
All kinematic data were log10 transformed prior to analyses to
meet the assumption of homoscedascity and normality for regression analyses
(Sokal and Rohlf, 1981;
Kachigan, 1991). To test for
differences in muscle mass between S. punctatus punctatus and other
lizards (see above), we used an analysis of co-variance with cranial length as
covariate. Bite force differences between S. punctatus and agamid
lizards were assessed using analysis of co-variance with head length as
covariate. Finally, differences in prey transport behavior were tested using
MANOVA coupled to univariate F-tests to explore which behavioral
elements differed between S. punctatus and Plocederma
stellio (Linnaeus 1758) (a generalized agamid lizard) (see
Herrel et al., 1996) of similar
body size (see results below).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) confirm
this finding (Fig. 2). In
contrast to lizards, S. punctatus appears to invest more muscle mass
into the pterygoideus group, which is also reflected in the presence of a
novel m. pterygoideus atypicus (Gorniak et
al., 1982) (Table
1).
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). Our
kinematic data show that S. punctatus needs an average of 11
transport cycles lasting 10.75 s to crush and transport a mealworm. Swallowing
was quicker and took only three cycles, lasting 4.6 s on average. Feeding
behavior in S. punctatus differs from that in agamid lizards of
similar size (Wilks' Lambda=0.254, F6,23=11.23;
P<0.001). S. punctatus is slower (transport stage
duration F1,28= 6.01; P=0.02) and tends to use
significantly more transport cycles (compared with P. stellio: seven
transport cycles), each of which lasts almost four times longer than in P.
stellio (1158 vs 365 m s–1, respectively;
F1,28=25.29; P<0.001) (see
Fig. 4). Unexpectedly, a
comparison of the relative gape cycle phase durations during transport (SO,
FO, FC and SC) (Table 3;
Fig. 5) demonstrated that
longer transport cycles were caused by increased duration of the entire
transport cycle rather than by an increase in specific phase durations. The
number of swallowing cycles needed and the swallowing phase durations,
however, are more similar in both species (P. stellio: three cycles
lasting 4.28 s on average). However, overall swallowing cycle duration is
still significantly longer in S. punctatus
(F1,28=6.29; P=0.02).
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Our static bite model indicates significant differences in the relative
participation of the different muscles groups in generating moments around the
jaw joint. Whereas the pterygoideus group comprises 40% of the total adductor
mass in S. punctatus, it generates only about 19% of the total moment
around the jaw joint. The external adductor by contrast generates 55% of the
total moment despite only being 42% of the total adductor mass. Interestingly,
the m. pterygoideus in P. stellio generates even less (9.8%) of the
jaw moment despite comprising nearly 54% of the total adductor mass
(Herrel et al., 1998a) (Tables
1 and
4).
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The orientation of the joint forces is also different in the two species.
For any given bite point or orientation of the food reaction forces, the angle
of the joint forces in S. punctatus tends to be slanted more anteriad
than in P. stellio where the orientation of the joint forces is more
consistently aligned with the quadrate
(Herrel et al., 1998b)
(Table 5). Together with a
counter-clockwise remaining moment (Table
6), these data suggest an anteriad compressive loading of the
quadrate onto the jugal in S. punctatus.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Moreover, juvenile S. punctatus bite less hard than lizards of
similar size. Although it is hard to extrapolate such data to other taxa, one
piece of evidence suggests that this may be a more general phenomenon.
Crocodylians, characterized by the presence of a lower temporal bar also bite
less hard on average than lizards of similar head lengths
(Herrel and Aerts, 2003) (A.H.,
unpublished data). The reduced bite force capacity in animals with a complete
lower arcade may have important implications for their efficiency in terms of
number of transport cycles and duration of a transport cycle while processing
food items. Indeed, in lizards, individuals with higher bite forces need fewer
cycles to crush and transport prey
(Verwaijen et al., 2002). To
determine whether high bite forces improve feeding efficiency in lizards
relative to S. punctatus, transport and swallowing kinematic data
were compared with data for P. stellio, an agamid lizard of similar
size, feeding on the same prey (Herrel et
al., 1996). Agamid lizards were considered to be an appropriate
comparison given their overall similarity in cranial and hyolingual morphology
(Schwenk, 2000).
Our data show that S. punctatus uses more transport cycles to
process arthropod prey, which also last longer on average. As they spend more
time on feeding (prey transport), less time is available for other behaviors
(e.g. defending territories, mating, etc.) suggesting a less `efficient'
feeding cycle in S. punctatus. However, despite being slower and
having lower bite forces, their unique propalineal jaw movement may allow
these animals to effectively shear and reduce relatively large food items
prior to swallowing. Our data support the hypothesis proposed by Rieppel and
Gronowski (Rieppel and Gronowski,
1981) that the loss of the lower temporal bar was associated with
an increase in bite force (i.e. lizards compared with S. punctatus),
and demonstrate how differences in skull structure like the loss of the lower
temporal bar may have considerable functional implications (increased bite
force, reduced feeding time). However, as an alternative to losing the lower
temporal arcade, a general bowing out of the arcade is observed in some
groups, thus providing additional space for the jaw adductor musculature in a
manner similar to the rounded zygomatic arches observed in mammals
(Turnbull, 1970). Whereas this
does provide additional space for jaw adductor muscles, the degree of bending
of the arch may be limited given that it is loaded in compression (see below),
which could result in too high stresses induced by biting. Clearly this needs
to be tested by finite element models and in vivo measurements of
strains in the lower temporal bar in S. punctatus.
The reduced bite force and feeding efficiency in animals with a complete
lower temporal bar may help explain the early loss of this trait in the fossil
record (Müller, 2003) and
the paucity of extant organisms showing this morphology. Indeed, the presence
of an intact lower temporal bar in the lepidosaur S. punctatus is
interpreted as derived due to the existence of many Triassic rhynchocephalians
with an incomplete bar (Carroll,
1985; Müller,
2003). Moreover, loss of the lower temporal bar may induce
mobility of the quadrate and may lead to complex intracranial movements as
observed in some lizards [e.g. geckoes
(Herrel et al., 1999b;
Herrel et al., 2000)].
However, this increased intracranial mobility in lizards is also associated
with the loss of additional cranial elements, thus making it unlikely to be
the driving force behind the loss of the lower temporal bar
(Herrel et al., 2007).
Rynchocephalia are characterized by an enlarged lateral palatine tooth row,
a feature not found in lizards. In the basal taxa, typically without a
complete lower temporal bar, this tooth row is oblique to the marginal
dentition but in the more derived spenodontines (also in eilenodontines), the
tooth row runs parallel (Jones,
2008). Consequently, the skull of S. punctatus differs
from that of all lizards in having two fixed rows of teeth on each side of the
upper jaw and one row of teeth on each side of the lower jaw
(Gorniak et al., 1982). This
special dentition pattern allows an interdigitation of tooth rows, rather than
interdigitation of teeth as observed in crocodilians for instance
(Cleuren and De Vree, 2000).
Additionally, S. punctatus uses a unique form of mandibular
translation to shear food rather than the typical puncture-crushing of lizards
(Gorniak et al., 1982;
Schwenk, 2000). This has been
suggested to date back to the pre-Triassic separation between sphenodontid
rhynchocephalians and carnivorous prolacertilians
(Robinson, 1973). The presence
of a lower temporal bar has been suggested to be associated with a shearing
bite and could, thus, be functionally related to this behavior and may
function to stabilize the quadrate (Lu et
al., 2008).
With respect to this hypothesis, our modelling data show that biting in
S. punctatus is typically associated with counter-clockwise moment
acting around the quadrato–squamosal junction. This tendency to rotate
the quadrate forwards upon contraction of the jaw adductors would be resisted
by the presence of a rigid lower temporal bar as observed in S.
punctatus and suggests that the lower temporal bar may indeed be linked
to the presence of the translational power stroke. This does, however, raise
the question as to why remaining moments in S. punctatus are always
counter–clockwise. One obvious difference in the jaw closing muscles
between S. punctatus and lizards is the presence of the m.
pterygoideus atypicus (Gorniak et al.,
1982; Wu, 2003).
Indeed, this muscle is positioned such that it would cause a tendency to
generate a counter-clockwise moment around the quadrato–squamosal joint
if the lower jaw were not allowed to slide forward. However, a simulation
where the m. pterygoideus atypicus is excluded from the static bite model in
S. punctatus, does not show marked differences in the orientation of
the joint forces and remaining moments. Thus, rather than being due solely to
the presence of the m. pterygoideus atypicus, the existence of a
counter-clockwise moment indicates a substantial rearrangement of the entire
jaw adductor complex.
Our model simulations also suggest that the orientation of the joint forces
in S. punctatus is variable and shows a tendency to be oriented in
front of the quadrate. The variability of the joint forces becomes especially
apparent when comparing our model output with a simulation for a lizard
(P. stellio) that does not take into account the jugomandibular
ligament (see Herrel et al.,
1998a). Indeed, for a similar range of food reaction force
orientations, the angles of the joint forces in P. stellio are
orientated more posteriad (between 80 and 120 deg.) (see
Table 5). Although speculative,
we suggest that the variable orientation of the joint forces in S.
punctatus could have resulted in the need for a broad and wide quadrate
base, which secondarily may have allowed the development of the unique sliding
joint of S. punctatus. In summary, our results suggest that the role
of the lower temporal bar may be tightly linked to the translational movement
of the lower jaw during the power stroke. Further analyses including finite
element models may prove especially insightful to further elucidate the
functional role of the lower temporal bar in S. punctatus.
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Acknowledgments |
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í Moravec for allowing us to dissect a
S. punctatus specimen from the collection at the Prague Natural
History Museum, Dr Z. Rocek for facilitating our stay in Prague, the staff at
the Otorohanga Kiwi house for help and support with this project. Supported by
a PhD grant of the Institute for the Promotion of Innovation through Science
and Technology in Flanders (IWT-Vlaanderen) to V.S. |
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