A dynamic model of mouth closing movements in clariid catfishes: the role of enlarged jaw adductors

Some species of Clariidae (air breathing catfishes) have extremely large (hypertrophied) jaw closure muscles. Besides producing higher bite forces, the enlarged muscles may also cause higher accelerations of the lower jaw during rapid mouth closure. Thus, jaw adductor hypertrophy could potentially also enable faster mouth closure. In this study, a forward dynamic model of jaw closing is developed to evaluate the importance of jaw adductor hypertrophy on the speed of mouth closure. The model includes inertia, pressure, tissue resistance and hydrodynamic drag forces on the lower jaw, which is modelled as a rotating half-ellipse. Simulations are run for four clariid species showing a gradual increase in jaw adductor hypertrophy (Clarias gariepinus, Clariallabes longicauda, Gymnallabes typus and Channallabes apus). The model was validated using data from high-speed videos of prey captures in these species. In general, the kinematic profiles of the fastest mouth closure from each species are reasonably well predicted by the model. The model was also used to compare the four species during standardized mouth closures (same initial gape angle, travel distance and cranial size). These simulations suggest that the species with enlarged jaw adductors have an increased speed of jaw closure (in comparison with the non-hypertrophied C. gariepinus) for short lower jaw rotations and when feeding at high gape angles. Consequently, the jaw system in these species seems well equipped to capture relatively large, evasive prey. For prey captures during which the lower jaw rotates freely over a larger distance before impacting the prey, the higher kinematic efficiency of the C. gariepinus jaw system results in the fastest jaw closures. In all cases, the model predicts that an increase in the physiological cross-sectional area of the jaw muscles does indeed contribute to the speed of jaw closure in clariid fish.     

It is all in the head: morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard

Males of the lizard Podarcis melisellensis occur in three distinct colours that differ in bite performance, with orange males biting harder than white or yellow ones. Differences in bite force among colour morphs are best explained by differences in head height, suggesting underlying variation in cranial shape and/or the size of the jaw adductors. To explore this issue further, we examined variation in cranial shape, using geometric morphometric techniques. Additionally, we quantified differences in jaw adductor muscle mass. No significant differences in size corrected head shape were found, although some shape trends could be detected between the colour morphs. Orange males have relatively larger jaw adductors than yellow males. Not only the mass of the external jaw adductors, but also that of the internal jaw adductors was greater for the orange morph. Data for other cranial muscles not related to biting suggest that this is not the consequence of an overall increase in robustness in orange individuals. These results suggest that differences in bite performance among morphs are caused specifically by an increase in the mass of the jaw adductor, which may be induced by differences in circulating hormone levels.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 13–22.     

Ontogenetic scaling of bite force in lizards and turtles

Because selection on juvenile life-history stages is likely strong, disproportionately high levels of performance (e.g., sprint speed, endurance, etc.) might be expected. Whereas this phenomenon has been demonstrated with respect to locomotor performance, data for feeding are scarce. Here, we investigate the relationships among body dimensions, head dimensions, and bite force during growth in lizards and turtles. We also investigate whether ontogenetic changes in bite performance are related to changes in diet. Our analyses show that, for turtles, head dimensions generally increase with negative allometry. For lizards, heads scale as expected for geometrically growing systems. Bite force generally increased isometrically with carapace length in turtles but showed significant positive allometry relative to body dimensions in lizards. However, both lizards and turtles display positive allometric scaling of bite force relative to some measures of head size throughout ontogeny, suggesting (1) strong selection for increased relative bite performance with increasing head size and (2) intrinsic changes in the geometry and/or mass of the jaw adductors during growth. Whereas our data generally do not provide strong evidence of compensation for lower absolute levels of performance, they do show strong links among morphology, bite force, and diet during growth.     

Size-related changes in cranial morphology affect diet in the catfish Clariallabes longicauda

Within the catfish family Clariidae, species exist with different degrees of jaw adductor hypertrophy. This jaw adductor hypertrophy has been related to bite performance, in turn suggesting a link to dietary specialization. Thus, an increase in the degree of hypertrophy will likely be reflected in an increase in the amount of hard prey in the diet. In the present study, we examine the ontogenetic scaling of cranial structure and diet in a species of catfish with a moderate degree of jaw adductor hypertrophy, Clariallabes longicauda . Additionally, we investigate whether the observed changes in the morphology of the feeding system during growth are linked to changes in diet. The fish examined demonstrate a strong positively allometric growth of the jaw adductors, of head height and of maximal head width, suggesting that larger fish can feed on larger and harder prey. Dietary data confirm these hypotheses and reveal an increase in maximal prey size consumed, the proportion of large prey in the diet, and average prey hardness during ontogeny. Moreover, the observed changes in the proportion of large prey consumed and prey hardness are correlated with an increase in lower jaw width and maximal head width, respectively. An increase in the amount of evasive prey in the diet with fish size is correlated with an increase in hyoid length. In summary, not only size dependent, but also size-independent variation of the feeding system was associated with ontogenetic changes in diet in C. longicauda .  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 323–334.     

Functional basis for sexual differences in bite force in the lizard Anolis carolinensis

In many species of lizards, males attain greater body size and have larger heads than female lizards of the same size. Often, the dimorphism in head size is paralleled by a dimorphism in bite force. However, the underlying functional morphological basis for the dimorphism in bite force remains unclear. Here, we test whether males are larger, and have larger heads and bite forces than females for a given body size in a large sample of Anolis carolinensis . Next, we test if overall head shape differs between the sexes, or if instead specific aspects of skull shape can explain differences in bite force. Our results show that A. carolinensis is indeed dimorphic in body and head size and that males bite harder than females. Geometric morphometric analyses show distinct differences in skull shape between males and females, principally reflecting an enlargement of the jaw adductor muscle chamber. Jaw adductor muscle mass data confirm this result and show that males have larger jaw adductors (but not jaw openers) for a given body and head size. Thus, the observed dimorphism in bite force in A. carolinensis is not merely the result of an increase in head size, but involves distinct morphological changes in skull structure and the associated jaw adductor musculature.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 111–119.     

Comparative study on the cranial morphology of Gymnallabes typus (Siluriformes: Clariidae) and their less anguilliform relatives,Clariallabes melas and Clarias gariepinus

We compare the cranial morphology of four fish species with an increasing anguilliformism in the following order: Clarias gariepinus, Clariallabes melas, Gymnallabes typus, and Channallabes apus. The main anatomical‐morphological disparities are the stepwise reduction of the skull roof along with the relative enlargement of the external jaw muscles, which occurred in each of them. Gymnallabes typus and C. apus lack a bony protection to cover the jaw muscles. The neurocranial bones of C. gariepinus, however, form a closed, broad roof, whereas the width of the neurocranium in C. melas is intermediate. Several features of the clariid heads, such as the size of the mouth and the bands of small teeth, may be regarded as adaptations for manipulating large food particles, which are even more pronounced in anguilliform clariids. The jaw musculature of G. typus is hypertrophied and attached on a higher coronoid process of the lower jaw, causing a larger adductive force. The hyomandibula interdigitates more strongly with the neurocranium and its dentition with longer teeth is posteriorly extended, closer to the lower jaw articulation. The anguilliform clariids also have their cranial muscles modified to enable a wider gape. The adductor mandibulae and the levator operculi extend more posteriorly, and the anterior attachment site of the protractor hyoidei dorsalis shifts toward the sagittal plane of the head. A phylogenetic analysis of the Clariidae, which is in progress, could check the validity of Boulenger's hypothesis that predecessors of the primitive fishes, such as Heterobranchus and most Clarias, would have evolved into progressively anguilliform clariids. J. Morphol. 240:169–194, 1999. © 1999 Wiley‐Liss, Inc.     

The effects of biting and pulling on the forces generated during feeding in the Komodo dragon (Varanus komodoensis)

In addition to biting, it has been speculated that the forces resulting from pulling on food items may also contribute to feeding success in carnivorous vertebrates. We present an in vivo analysis of both bite and pulling forces in Varanus komodoensis, the Komodo dragon, to determine how they contribute to feeding behavior. Observations of cranial modeling and behavior suggest that V. komodoensis feeds using bite force supplemented by pulling in the caudal/ventrocaudal direction. We tested these observations using force gauges/transducers to measure biting and pulling forces. Maximum bite force correlates with both body mass and total body length, likely due to increased muscle mass. Individuals showed consistent behaviors when biting, including the typical medial-caudal head rotation. Pull force correlates best with total body length, longer limbs and larger postcranial motions. None of these forces correlated well with head dimensions. When pulling, V. komodoensis use neck and limb movements that are associated with increased caudal and ventral oriented force. Measured bite force in Varanus komodoensis is similar to several previous estimations based on 3D models, but is low for its body mass relative to other vertebrates. Pull force, especially in the ventrocaudal direction, would allow individuals to hunt and deflesh with high success without the need of strong jaw adductors. In future studies, pull forces need to be considered for a complete understanding of vertebrate carnivore feeding dynamics.     

Scaling of suction feeding performance in the catfish Clarias gariepinus

Ontogenetic changes in the absolute dimensions of the cranial system together with changes in kinematics during prey capture can cause differences in the spatiotemporal patterns of water flow generated during suction feeding. Because the velocity of this water flow determines the force that pulls prey toward and into the mouth cavity, this can affect suction feeding performance. In this study, size-related changes in the suction-induced flow patterns are determined. To do so, a mathematical suction model is applied to video recordings of prey capturing Clarias gariepinus ranging in total length from 111 to 923 mm. Although large C. gariepinus could be expected to have increasing peak velocities of water flow compared with small individuals, the results from the hydrodynamic model show that this is not the case. Yet, when C. gariepinus becomes larger, the expansive phase is prolonged, resulting in a longer sustained flow. This flow also reaches farther in front of the mouth almost proportionally with head size. Forward dynamical simulations with spherical prey that are subjected to the calculated water flows indicate that the absolute distance from which a given prey can be sucked into the mouth as well as the maximal prey diameter increase substantially with increasing head size. Consequently, the range of potential prey that can be captured through suction feeding will become broader during growth of C. gariepinus. This appears to be reflected in the natural diet of this species, where both the size and the number of evasive prey increase with increasing predator size.     

Interspecific variation in sternohyoideus muscle morphology in clariid catfishes: functional implications for suction feeding

Depression of the hyoid apparatus plays a crucial role in generating suction, especially in fishes with a dorso-ventrally flattened head shape. It is generally assumed that shortening of the sternohyoideus muscle, which connects the hyoid to the pectoral girdle, contributes to hyoid depression. However, a recent study on the clariid catfish Clarias gariepinus has shown that this muscle does not shorten but elongates during this phase through retraction of the pectoral girdle. Here, we test whether this pattern is general among clariid catfish, or if variation in the morphology of the sternohyoideus may result in a different sternohyoideus behavior during hyoid depression. First, sternohyoideus mass, effective cross-sectional area, fiber length and fiber diameter were measured and compared for four clariid species. Next, velocity and magnitude of hyoid depression during prey capture (from high-speed videos), as well as patterns of sternohyoideus strain were analyzed (from high-speed X-ray videos) in these species. While morphology and hyoid depression performance varied considerably among these species, only the species with the most massive sternohyoideus, Gymnallabes typus, showed shortening of the sternohyoideus muscle during the initial part of the expansive phase. The data for Channallabes apus demonstrate that increasing the magnitude of hyoid depression does not necessarily require a shortening of the m. sternohyoideus, as it shows elongation of this muscle during hyoid depression.     

Evolution of bite performance in turtles

Abstract Among vertebrates, there is often a tight correlation between variation in cranial morphology and diet. Yet, the relationships between morphological characteristics and feeding performance are usually only inferred from biomechanical models. Here, we empirically test whether differences in body dimensions are correlated with bite performance and trophic ecology for a large number of turtle species. A comparative phylogenetic analysis indicates that turtles with carnivorous and durophagous diets are capable of biting harder than species with other diets. This pattern is consistent with the hypothesis that an evolutionary increase in bite performance has allowed certain turtles to consume harder or larger prey. Changes in carapace length tend to be associated with proportional changes in linear head dimensions (no shape change). However, maximum bite force tends to change in proportion to length cubed, rather than length squared, implying that changes in body size are associated with changes in the design of the jaw apparatus. After the effect of body size is accounted for in the analysis, only changes in head height are significantly correlated with changes in bite force. Additionally, our data suggest that the ability to bite hard might trade off with the ability to feed on fast agile prey. Rather than being the direct result of conflicting biomechanical or physiological demands for force and speed, this trade‐off may be mediated through the constraints imposed by the need to retract the head into the shell for defensive purposes.     

Morphometric and allozyme variation in the African catfishes Clarias gariepinus and C. anguillaris

This study investigated morphological characters and electrophoretic polymorphism at 25 protein loci in nine wild populations of the African clariid catfish Clarias gariepinus and seven wild populations of C. anguillaris. Two other clariid species, Clarias albopunctatus and Heterobranchus longifilis , were used as outgroups in the allozyme study. Morphometric and allozyme data are congruent for the Nilo-Sudanian populations of C. gariepinus and C. anguillaris. Both approaches also distinguished two groups amongst the C. gariepinus populations, one containing Nilo-Sudanian populations and the other including Lake Victoria and southern African populations. However, allozyme data suggest that C. gariepinus is not a monophyletic group and show that C. albopunctatus is more divergent from C. gariepinus and C. anguillaris than it is from H. longifilis , stressing the need for a revision of clariid systematics. The variation observed in C. gariepinus is discussed in terms of palaeogeographical events and its use in aquaculture.     

Comparative bite forces and canine bending strength in feline and sabretooth felids: implications for predatory ecology

The sabretooth felids were widespread across much of the world in the Late Tertiary, and appear to have been an important group of large predators. Owing to the substantially different skull morphology of derived sabretooths compared with extant felids, there has been considerable debate over the killing mode, bite forces, and bending strength of the large upper canines, and over the implications of these characteristics on feeding ecology. Debates have, however, usually been based on indirect comparisons of force vectors. In this paper, I provide assessments of the estimated force output from the jaw adductor muscles, based on estimates of muscle cross-sectional areas and force vectors, along with canine bending strengths, in a variety of sabretooth felids, in comparison with extant felids. In general, sabretoothed felids had moderately powerful bites, albeit with less jaw adductor power for their body sizes compared with extant felids, sometimes markedly so. Less derived sabrecats appear to have had proportionally higher bite forces than derived forms. The length of the upper canines seemingly compromised their bending strength at any given body size, and again this was most marked in derived forms. However, compared with estimated jaw adductor forces, the canines of sabrecats appear, if anything, to have been stronger than those of extant conical-toothed felids. It has previously been suggested that large sabretoothed felids hunted large prey with a canine shearing bite, powered in part by the jaw adductors and in part by the muscles of the upper neck–occipital region. The present results of canine bending strengths versus the predicted bite force from the jaw adductors supports this suggestion.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 151 , 423–437.     

Feeding biomechanics and theoretical calculations of bite force in bull sharks (Carcharhinus leucas) during ontogeny

Evaluations of bite force, either measured directly or calculated theoretically, have been used to investigate the maximum feeding performance of a wide variety of vertebrates. However, bite force studies of fishes have focused primarily on small species due to the intractable nature of large apex predators. More massive muscles can generate higher forces and many of these fishes attain immense sizes; it is unclear how much of their biting performance is driven purely by dramatic ontogenetic increases in body size versus size-specific selection for enhanced feeding performance. In this study, we investigated biting performance and feeding biomechanics of immature and mature individuals from an ontogenetic series of an apex predator, the bull shark, Carcharhinus leucas (73–285 cm total length). Theoretical bite force ranged from 36 to 2128 N at the most anterior bite point, and 170 to 5914 N at the most posterior bite point over the ontogenetic series. Scaling patterns differed among the two age groups investigated; immature bull shark bite force scaled with positive allometry, whereas adult bite force scaled isometrically. When the bite force of C. leucas was compared to those of 12 other cartilaginous fishes, bull sharks presented the highest mass-specific bite force, greater than that of the white shark or the great hammerhead shark. A phylogenetic independent contrast analysis of anatomical and dietary variables as determinants of bite force in these 13 species indicated that the evolution of large adult bite forces in cartilaginous fishes is linked predominantly to the evolution of large body size. Multiple regressions based on mass-specific standardized contrasts suggest that the evolution of high bite forces in Chondrichthyes is further correlated with hypertrophication of the jaw adductors, increased leverage for anterior biting, and widening of the head. Lastly, we discuss the ecological significance of positive allometry in bite force as a possible “performance gain” early in the life history of C. leucas.     

Sexual dimorphism,body size,bite force and male mating success in tuatara

Sexual dimorphisms in body size and head size are common among lizards and are often related to sexual selection on male fighting capacity (organismal performance) and territory defence. However, whether this is generally true or restricted to lizards remains untested. Here we provide data on body and head size, bite performance and indicators of mating success in the tuatara (Sphenodon punctatus), the closest living relative to squamates, to explore the generality of these patterns. First, we test whether male and female tuatara are dimorphic in head dimensions and bite force, independent of body size. Next, we explore which traits best predict bite force capacity in males and females. Finally, we test whether male bite force is correlated with male mating success in a free‐ranging population of tuatara (Sphenodon punctatus). Our data confirm that tuatara are indeed dimorphic in head shape, with males having bigger heads and higher bite forces than females. Across all individuals, head length and the jaw closing in‐lever are the best predictors of bite force. In addition, our data show that males that are mated have higher absolute but not relative bite forces. Bite force was also significantly correlated to condition in males but not females. Whereas these data suggest that bite force may be under sexual selection in tuatara, they also indicate that body size may be the key trait under selection in contrast to what is observed in squamates that defend territories or resources by biting. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 287–292.     

草原蜥两性的咬合力及头部形态特征比较

咬合力作为衡量动物生存能力的重要指标,可以在一定程度上反映动物捕食、反捕食和争夺配偶的能力。对于蜥蜴类动物而言,头部形态和咬合力大小之间常呈现显著线性关系。通过测量2018年7月采集于新疆霍城县图开沙漠的24号草原蜥(Trapelussanguinolenta)(雌13,雄11)的头部形态指标,并使用薄膜压力测试仪测定咬合力,采用单因素方差分析(ANOVA)、主成分分析、模型拟合及逐步回归4种方法探究草原蜥咬合力的两性差异及其与头部形态指标的关系。结果表明,草原蜥头体长、头长、头宽、头高、口宽和下颌长在两性个体间均无显著差异,草原蜥两性个体之间咬合力也没有显著差异。主成分分析及赤池信息模型拟合结果均显示,头长、头宽和下颌长是影响草原蜥咬合力的重要因素,逐步回归分析揭示草原蜥的咬合力主要受头宽影响。上述研究结果表明,草原蜥的咬合力受头部形态大小的影响,但两性个体之间咬合力却不存在显著差异,这与头部形态特征未表现出两性差异一致,这可能是草原蜥对灌丛生活的适应,具体而言,是头部大小与运动权衡的结果。     

Cranial morphology and bite force in Chamaeleolis lizards--adaptations to molluscivory?

Anolis lizards have become a model system for the study of adaptive radiations as species with similar morphologies occupying similar habitats have arisen independently on all the larger islands in the Caribbean. However, on both, Cuba and Hispaniola unique forms have evolved that seemingly have no counterparts on any of the other Caribbean islands. Anoles of the genus Chamaeleolis comprise such a unique form and have been termed 'twig giants' because of their cryptic life style, slow locomotor mode, and short limbs. However, some of the most unusual features of these lizards are their large heads and molluscivorous diet. Here, we compare head shape, bite force, and muscle structure among sexes and age classes of Chamaeleolis lizards with Anolis crown giants. Our data show that Chamaeleolis lizards have a dramatically different head shape characterized by tall heads with a pronounced temporal ridge and long snouts. Analyses of bite force, surprisingly, show no differences between adult Chamaeleolis and Anolis crown giants. Juveniles of Chamaeleolis, however, have very tall heads for their size and bite harder than Anolis juveniles do. This can be related to the propensity of juveniles of this genus to eat snails, food items for which high bite forces are crucial. This observation is corroborated by the presence of well-developed jaw adductors in juveniles. Thus, our data suggest that the unusual phenotype of adults with large and tall heads may be due to selection on the juvenile life history stages.     

Musculoskeletal underpinnings to differences in killing behavior between North American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae)

Accipiters (Accipiter spp.) and falcons (Falco spp.) both use their feet to seize prey, but falcons kill primarily with their beaks, whereas accipiters kill with their feet. This study examines the mechanistic basis to differences in their modes of dispatching prey, by focusing on the myology and biomechanics of the jaws, digits, and distal hindlimb. Bite, grip, and distal hindlimb flexion forces were estimated from measurements of physiological cross-sectional area (PCSA) and indices of mechanical advantage (MA) for the major jaw adductors, and digit and tarsometatarsal flexors. Estimated bite force, total jaw adductor PCSA, and jaw MA (averaged over adductors) tended to be relatively and absolutely greater in falcons, reflecting their emphasis on biting for dispatching their prey. Differences between genera in estimated grip force, total digit flexor PCSA, and digit MA (averaged over inter-phalangeal joints and digits) were not as clear-cut; each of these parameters scaled positively allometric in accipiters, which may reflect the scaling of both prey size, and the proportion of mammalian prey consumed by this lineage with increasing body size. Estimated tarsometatarsal force was greater in falcons than in accipiters, due to their greater MA, which may reflect selection for incurring greater forces during prey strikes. Conversely, the comparatively lower tarsometatarsal MA in accipiters reflects their capacity for greater foot speed potentially necessary for grasping elusive prey. Thus, this study elucidates how differences in jaw and hindlimb musculoskeletal morphology of accipiters and falcons are reflected in differences in their killing modes, and through differences in their force-generating capacities.     

Effects of gape and tooth position on bite force and skull stress in the dingo (Canis lupus dingo) using a 3-dimensional finite element approach

Models of the mammalian jaw have predicted that bite force is intimately linked to jaw gape and to tooth position. Despite widespread use, few empirical studies have provided evidence to validate these models in non-human mammals and none have considered the influence of gape angle on the distribution of stress. Here using a multi-property finite element (FE) model of Canis lupus dingo, we examined the influence of gape angle and bite point on both bite force and cranial stress. Bite force data in relation to jaw gape and along the tooth row, are in broad agreement with previously reported results. However stress data showed that the skull of C. l. dingo is mechanically suited to withstand stresses at wide gapes; a result that agreed well with previously held views regarding carnivoran evolution. Stress data, combined with bite force information, suggested that there is an optimal bite angle of between 25 degrees and 35 degrees in C. l. dingo. The function of these rather small bite angles remains unclear.     

Carnivory maintains cranial dimorphism between males and females: Evidence for niche divergence in extant Musteloidea

The evolution and maintenance of sexual dimorphism has long been attributed to sexual selection. Niche divergence, however, serves as an alternative but rarely tested selective pressure also hypothesized to drive phenotypic disparity between males and females. We reconstructed ancestral social systems and diet and used Ornstein–Uhlenbeck (OU) modeling approaches to test whether niche divergence is stronger than sexual selection in driving the evolution of sexual dimorphism in cranial size and bite force across extant Musteloidea. We found that multipeak OU models favored different dietary regimes over social behavior and that the greatest degree of cranial size and bite force dimorphism were found in terrestrial carnivores. Because competition for terrestrial vertebrate prey is greater than other dietary groups, increased cranial size and bite force dimorphism reduces dietary competition between the sexes. In contrast, neither dietary regime nor social system influenced the evolution of sexual dimorphism in cranial shape. Furthermore, we found that the evolution of sexual dimorphism in bite force is influenced by the evolution of sexual dimorphism in cranial size rather than cranial shape. Overall, our results highlight niche divergence as an important mechanism that maintains the evolution of sexual dimorphism in musteloids.