Implications of FE stress distributions for feeding ecology in the Komodo dragon
Given that, for two equivalently loaded structures, the one with lower and more dispersed stress will resist higher loads before catastrophic failure (Rayfield et al. 2001; Fastnacht et al. 2002; Rayfield, 2004, 2005; Preuschoft & Witzel, 2005; Moreno et al. 2007), we conclude that overall lower stresses exhibited in distal normal, lateral-pull, and mesial pull-back bites suggest that the skull of V. komodoensis is best adapted to perform these feeding behaviours.
These simulations demonstrate that overall skull stress magnitudes are mainly a consequence of mandibular load (Figs 2 and 3). During a distal bite the out-lever (muscle- to bite-position) is reduced. This also decreases mandibular torsion, because a restraint closer to the jaw joint will inhibit medial rotation caused by off-centre muscle tensile force (Smith, 1982). This bending reduction moderates general stress in normal and pull-back bites. However, the presence of an extrinsic 50 N lateral tensile force counteracts bending in the mesial lateral-pull model. This extrinsic force reduces medial torsion of the mandible and quadrate-articular joint compression because of reduction in mandible outward bending (wishboning). Stress distribution in the posterior cranium is focused in the quadrate, squamosal, and pterygoid in both normal and pull-back bites. Substantial force is also received by the squamosal-quadrate joint. This may be a consequence of rigidity in the modelled quadrate-articular joint and limited m. pterygoideus quadrate-articular joint stabilization (see below). Consequently, our simulations of squamosal-quadrate deformation probably overestimate stress. However, despite the presence of these model artefacts, it is reasonable to suggest that the squamosal-quadrate joint will be under some flexion/extension loading due to the presence of streptostylic movement (Frazzetta, 1962, Metzger, 2002).
The pterygoid bone is stressed mainly in response to relatively large m. pterygoideus force production. However, we found different mechanical behaviour in the pterygoid depending on the presence/absence of longitudinal extrinsic loads. In normal bite simulations (absence of extrinsic loads), the epipterygoid-pterygoid joint is bent laterally via muscle tension action. In contrast, in pull-back simulations (presence of longitudinal extrinsic load) the epipterygoid-pterygoid joint is posteriorly flexed as the skull is pulled anteriorly and m. pterygoideus tension is counterbalanced.
Modelling limitations must be considered before further interpretation of these results. Our simulation of the m. pterygoideus comprises seven pretensioned trusses distributed in an equal number of muscle action lines (Fig. 1, Table 1). Although this architecture represents an improvement on the commonly used single point load (Strait et al. 2002; Dumont et al. 2005; Strait et al. 2006), it may still underestimate m. pterygoideus force and function. Our modelled m. pterygoideus does not simulate wrapping morphology nor does it fully replicate muscle pennation. Furthermore, in life the pterygoid is under more complex loads than any simulated here. Protractor and levator pterygoideus muscles, although proportionally much smaller (hence not included in the model), control some of the m. pterygoideus induced lateral bending and epipterygoid-pterygoid joint flexion generated by extrinsic longitudinal forces. These influences could reduce pterygoid stress. However, the m. pterygoideus also plays an important role restraining intra-mandibular joint flexion. This flexion function was not included in our modelled mandible, but in life it would transmit extra loads to the pterygoid complex. Consequently, the stress shown about the pterygoid, regardless of model limitations, is also likely to be high in real conditions.
High stress is located in the rostrum near the restraints in distal normal and mesial pull-back simulations, but is not observed in mesial normal and distal pull-back load cases. As explained above, this is mainly a consequence of the way in which the mandible is loaded, which not only results in lower overall stress, but also application of a greater bite force. Note that mesial normal loading produces almost 45% less bite force, but reveals similar stress magnitudes to the distal normal loading. Hence, a mesial normal bite is weak relative to a distal normal bite.
Regarding pull-back load cases, of particular interest is our observation that although mesial pull-back loading generates 20% less force, in this case the skull is under 20% less stress than during distal pull-back loading. Therefore, considering these proportions and the linearity of the model, a distal pull-back would apply equivalent bite force to that of a mesial pull-back load without increasing skull stress. This key feature of performance in the skull of V. komodoensis strongly suggests that the structure is far better optimized to simultaneously apply a jaw adductor-driven bite and postcranially generated pull-back, as opposed to a solely jaw driven (normal) bite.
This conclusion is further supported by clear evidence for multiple adaptations facilitating the rearward distribution of the loads in both symmetric and asymmetric bites. These include the triangular shape of the maxilla and its proximal and elongated contact surface with the frontal, which distribute the compressive force generated when biting toward the frontal and parietal; light anterior skull construction in comparison with the posterior one; and forward direction of the splenial-dentary suture, which easily transmit loads to the rest of the mandible. Additionally, the m. adductor mandibulae and m. pseudotemporalis contribute to mandibular retraction/protraction, due to largely dorsoposteriorly/ventroanteriorly orientation of muscle fibres. Only a small portion of the m. adductor mandibulae is dorsoventrally oriented (MAEMa). Together with the m. pseudotemporalis profundus, also a minor muscle, these are the main mandibular elevators.
During a lateral-pull, high stress is distributed in the prootic, parietal, prefrontal and nasal bones as well as in the squamosal, quadrate and pterygoid. This is likely because the lateral extrinsic force applied on the maxilla produces a compressive force against the prefrontal, septomaxilla and nasal in the biting side. Moreover, consequent lateral bending of the mandible generates a large lateral bending in the squamosal-quadrate joint, which is extended toward the prootic. Model artefacts discussed above may have amplified this effect. Also, lateral bending of the mandible produces posterior flexion of the epipterygoid-pterygoid joint, protracting the rostrum.
Our modelling suggests that the V. komodoensis skull is poorly adapted to resist a lateral-pull bite. Although the heterogeneous model accounts for differences in material properties within the bone, it does not include connective tissue, which in life might further reduce overall stress (and see below). Uncertainty exists regarding just how much reduction this would imply. However, comparisons made between distal and mesial bites within the same model, indicate that a mesial lateral-pull bite generates 20% larger force, whereas a distal one produces 20% less overall stress. This means that distal and mesial bites are proportionally equivalent under linear conditions and that the Komodo dragon could be equally adapted for a lateral-pull at any bite point. Our modelling further suggests that the skull can withstand large asymmetrical loads without compromising the overall structure.
Additional differences in bone performance were observed between heterogeneous and homogeneous models. Homogeneous modelling reveals equivalent heterogeneous high stress zones, but also produces expanded stress areas. These zones amplify overall stress. The only cases in which this difference diminishes are in mesial pulling bites (lateral as well as pull-back). These results relate directly to the lower stiffness and thin contact of the premaxilla-maxilla suture. This is best exemplified in stress distribution under distal pull-back loading, which shows more proximally extended tensile stress in the anterior maxilla and greater compression in the premaxilla in the heterogeneous relative to the homogeneous model (Fig. 3). A real skull might present even more marked tensile/compressive patterns because of variation in material properties of the bone and other connective tissues. We may also expect to see a degree of functional compartmentalization in different skull regions and structures, and consequent ‘insulation’ against high loads (Rafferty & Herring, 1999; Herring & Teng, 2000; Rafferty et al. 2003).
Our data are consistent with the animal's documented defleshing techniques, particularly with respect to the relative motion of the rostrum. When processing a carcass, V. komodoensis rotates the muzzle in both the lateral and posterior directions simultaneously (Auffenberg, 1981). This results in varied direction and intensity of forces along the muzzle.
In addition to securing the prey item, the distal teeth are the first to enter the substrate and are closest to the occiput. These teeth are drawn mostly in the posterior direction with relatively little lateral movement, but larger bite force. Conversely, the mesial teeth are further away from the occiput and are laterally and posteriorly driven by a combination of rotational neck movements and full body longitudinal tensile force (pull-back). Our data indicates that the occiput is better suited to withstand forces in the direction of pull-back loading, whereas anteriorly, the skull performs better for a lateral-pull with a far more evenly distributed load along the rostrum.
We conclude that in large part our FE model of the Komodo dragon skull faithfully reproduces qualitative observational data on feeding behaviour of the animal. This in turn suggests that similar techniques can be applied to assist in the prediction of behaviour for taxa of unknown habits, both living and extinct. Models such as those generated in the present study may be useful in the study of a range of further questions, such as the role of cranial kinesis in varanids and other reptiles (work in progress).
Comparison with other extant and extinct taxa
Our estimates of muscle force generated by V. komodoensis mandible adductors were surprisingly low (90 N each side, Table 1) for a 1.6-m-long lizard. The alignment of muscle fibres, mostly at an acute angle to the mandible, together with the low modelled gape (15º), are likely to have further contributed to weak bite reaction forces. Maximum bite force obtained was around 10–20 N. However, if the same model had a larger gape, the muscle would have gained extra mechanical advantage and larger moments in the jaw articulation would have produced stronger bites. The animal might also have been capable of generating large angular accelerations to the jaw at the beginning of a snapping bite (Sinclair & Alexander, 1987). Other factors acting to reduce bite reaction forces in the model include the slightly protracted quadrate orientation and elastic deformation of interdental beams. Moreover, the storage of strain energy in more elastic regions of our heterogeneous model is likely to have resulted in a reduction of force available at bite points (Wroe et al. 2007b). However, although consideration of these complicating factors suggests that bite reaction forces taken from our model may be sub-maximal, results of estimates using 2D techniques together with in vivo data from captive V. komodoensis strongly imply that our 3D-based predictions do not greatly underestimate bite force.
Using 2D methodology to predict bite forces in a much smaller varanid (V. bengalensis – 2.6 kg body mass, 5 cm head length), Sinclair & Alexander (1987), obtained forces of 5 N–13 N in vertical mesial and distal bite positions respectively. Applying this 2D calculation to our much larger V. komodoensis specimen gives bite reaction forces of 11 N and 16 N at the same bite points. The weak bite of the Komodo dragon may be in part explained by the fact that its condyle is positioned more anteriorly than that of Varanus bengalensis, conferring relative mechanical advantage to the latter.
Herrel et al. (1999a) measured ~2.38–109 N in vivo bite force for specimens of the lizard Gallotia galloti ranging from 1.5 to 3 cm in head length. The skull of this species is around 23–26% of the snout-vent length (SVL), while the head length of the V. komodoensis we studied is only 15% of SVL. In comparing estimated bite forces between different species, including small crocodiles and turtles, Sinclair & Alexander (1987) concluded that varanids in general produced comparatively small bite forces among Reptilia.
Thus, overall, our results are consistent with previous findings that varanids produce relatively weak bite reaction forces, and further, that bite force in the Komodo dragon is weak among varanids.
With respect to pulling forces, gauge data obtained from two captive V. komodoensis (specimens 98R046 and 98R069, Miami Metro Zoo) with similar head length (~16 cm) to the one modelled in the present study (14 cm), indicate that they are capable of exerting forces exceeding the equivalent of half their body mass (~170 N). These specimens were fed regularly, and appeared to be relatively sated. Increased hunger might reasonably result in higher level of ‘enthusiasm’ and higher pull forces. These results suggest that postcranial musculature in the Komodo dragon is capable of delivering forces that may exceed those of the jaw elevators by an order of magnitude or more.
Nonetheless, jaw adductor-driven bite force is a factor to be considered in the understanding of predatory behaviour in any carnivorous vertebrate. A well-demonstrated relationship between bite force and feeding ecology has been established among extant mammalian carnivores (Wroe et al. 2005; Christiansen & Wroe, 2007). These authors observe that this cannot be considered a universal relationship where taxa under consideration exhibit unique adaptations, even within Mammalia. Wroe et al. (2005) predicted relatively low bite force in the highly specialized fossil sabrecat Smilodon fatalis, but concluded that this indicated unique killing behaviour, wherein a combination of extraordinary tooth morphology and the recruitment of cervical musculature facilitated predation tactics unknown among living cats. Extant felids typically deploy a crushing bite to the posterior cranium or cervical vertebra in small- to medium-sized prey, or a prolonged suffocating bite to the neck of large prey. In contrast, it is likely that S. fatalis rarely took small-medium prey and applied a ‘canine-shear bite’ to soft tissues of large prey that produced major trauma and a quick kill (McHenry et al. 2007), an obvious advantage being minimization of physical threat to the predator. Broad analogy has been made between this approach and that of V. komodoensis (Akersten, 1985).
Varanus komodoensis shares anatomical features with some theropod dinosaurs, such as Allosaurus and the abelisaurid Majungasaurus. All have serrated blade-like teeth, gracile well-fenestrated skulls, and long rostra. A notable difference is that relative to V. komodoensis, these dinosaurs have laterally compressed crania (taller than wide), and consequently might be expected better to resist dorsoventral loads. We also predict that differences between working and balancing sides will be less marked than is evident in the dorsoventrally compressed cranium of the Komodo dragon. On the other hand, reconstruction of tyrannosaurid neck musculature by Snively & Russell (2007) suggests that tyrannosaurids, with broad dental arcades and high leverage for lateroflexive neck muscles, could have engaged in a similar defleshing technique to that of V. komodoensis. In some ways these tyrannosaurids, as well as extant crocodilians, may represent a closer comparison to the Komodo dragon than other tall-skulled carnivorous archosaurs. However, their more robust cranial and dental morphology also suggests different mechanical and feeding behaviour in other respects (Rayfield, 2004, 2007; Barrett & Rayfield, 2006; McHenry et al. 2006; Snively et al. 2006) that probably involved more puncture-and-tear excision of flesh than the efficient slicing evident in the Komodo dragon.