Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata).

The southern alligator lizard (Elgaria multicarinata) exhibits a courtship behaviour during which the male firmly grips the female's head in his jaws for many hours at a time. This extreme behaviour counters the conventional wisdom that reptilian muscle is incapable of powering high-endurance behaviours. We conducted in situ experiments in which the jaw-adductor muscles of lizards were stimulated directly while bite force was measured simultaneously. Fatigue tests were performed by stimulating the muscles with a series of tetanic trains. Our results show that a substantial sustained force gradually develops during the fatigue test. This sustained force persists after peak tetanic forces have declined to a fraction of their initial magnitude. The observed sustained force during in situ fatigue tests is consistent with the courtship behaviour of these lizards and probably reflects physiological specialization. The results of molecular analysis reveal that the jaw muscles contain masticatory and tonic myosin fibres. We propose that the presence of tonic fibres may explain the unusual sustained force properties during mate-holding behaviour. The characterization of muscle properties that facilitate extreme performance during specialized behaviours may reveal general mechanisms of muscle function, especially when done in light of convergently evolved systems exhibiting similar performance characteristics.

Reliable quantification of bite-force performance requires use of appropriate biting substrate and standardization of bite out-lever.

Bite-force performance is an ecologically important measure of whole-organism performance that shapes dietary breadth and feeding strategies and, in some taxa, determines reproductive success. It also is a metric that is crucial to testing and evaluating biomechanical models. We reviewed nearly 100 published studies of a range of taxa that incorporate direct in vivo measurements of bite force. Problematically, methods of data collection and processing vary considerably among studies. In particular, there is little consensus on the appropriate substrate to use on the biting surface of force transducers. In addition, the bite out-lever, defined as the distance from the fulcrum (i.e. jaw joint) to the position along the jawline at which the jaws engage the transducer, is rarely taken into account. We examined the effect of bite substrate and bite out-lever on bite-force estimates in a diverse sample of lizards. Results indicate that both variables have a significant impact on the accuracy of measurements. Maximum bite force is significantly greater using leather as the biting substrate compared with a metal substrate. Less-forceful bites on metal are likely due to inhibitory feedback from mechanoreceptors that prevent damage to the feeding apparatus. Standardization of bite out-lever affected which trial produced maximum performance for a given individual. Indeed, maximum bite force is usually underestimated without standardization because it is expected to be greatest at the minimum out-lever (i.e. back of the jaws), which in studies is rarely targeted with success. We assert that future studies should use a pliable substrate, such as leather, and use appropriate standardization for bite out-lever.

Sustained force production by the jaw-adductor muscles of a megalophagous frog, Ceratophrys cranwelli.

Most frogs have weak jaws that play a relatively minor role in tongue-mediated prey capture. Horned frogs (Ceratophrys spp.), however, follow the projection of a large tongue with a vice-like grip of their jaws to hold and immobilize prey. Prey include relatively large vertebrates, which they may restrain for minutes to possibly hours. High endurance behaviors, such as prolonged biting, require that muscles be capable of sustained force production. The feeding behavior of Ceratophrys suggests that their jaw-adductor muscles may be capable of powering sustained bites for long periods. We examined the capacity for sustained bite force by conducting an in situ experiment during which we measured bite force while bilaterally and supramaximally stimulating the jaw-adductor muscles of euthanized Cranwell's horned frogs (C. cranwelli). Muscles were stimulated for at least 60 min with a series of tetanic trains, with one experiment lasting over 6 h. We found that a significant sustained force develops during the first few minutes of the experiment, and this force is present between tetanic trains when the muscles are not being stimulated. The sustained force persists long after tetanic forces are barely detectable. The observed sustained force phenomenon parallels that observed for the jaw-adductor muscles of alligator lizards (Elgaria), another animal capable of sustained biting. The ability to bite with sustained and significant force by C. cranwelli may be facilitated by a configuration of different muscle fiber types, such as slow tonic fibers, as well as specializations in the muscle fibers that mitigate the effects of fatigue.

Female-female aggression in the Gila monster (Heloderma suspectum).

Historically, the role of aggression in the social lives of animals overwhelmingly focused on males. In recent years, however, female-female aggression in vertebrates, particularly lizards, has received increasing attention. This growing body of literature shows both similarities and differences to aggressive behaviours between males. Here, we document female-female aggression in captive Gila monsters (Heloderma suspectum). Based on four unique dyadic trials (eight adult female subjects), we developed a qualitative ethogram. Unexpected and most intriguing were the prevalence and intensity of aggressive acts that included brief and sustained biting, envenomation, and lateral rotation (i.e. rolling of body while holding onto opponent with closed jaws). Given specific behavioural acts (i.e. biting) and the results of bite-force experiments, we postulate that osteoderms (bony deposits in the skin) offer some degree of protection and reduce the likelihood of serious injury during female-female fights. Male-male contests in H. suspectum, in contrast, are more ritualized, and biting is rarely reported. Female-female aggression in other lizards has a role in territoriality, courtship tactics, and nest and offspring guarding. Future behavioural research on aggression in female Gila monsters is warranted to test these and other hypotheses in the laboratory and field.

Thermal effects on the dynamics and motor control of ballistic prey capture in toads: maintaining high performance at low temperature.

Temperature has a strong influence on biological rates, including the contractile rate properties of muscle and thereby the velocity, acceleration and power of muscle-powered movements. We hypothesized that the dynamics of movements powered by elastic recoil have a lower thermal dependence than muscle-powered movements. We examined the prey capture behavior of toads (Bufo terrestris) using high speed imaging and electromyography to compare the effects of body temperature (11-35°C) on the kinematics, dynamics and motor control of two types of movement: (1) ballistic mouth opening and tongue projection, which are powered by elastic recoil, and (2) non-ballistic prey transport, including tongue retraction and mouth closing, which are powered directly by muscle contraction. Over 11-25°C, temperature coefficients of ballistic mouth opening and tongue projection dynamics (Q(10) of 0.99-1.25) were not significantly different from 1.00 and were consistently lower than those of prey transport movements (Q(10) of 1.77-2.26), supporting our main hypothesis. The depressor mandibulae muscle, which is responsible for ballistic mouth opening and tongue projection via the recovery of elastic strain energy stored by the muscle prior to the onset of the movement, was activated earlier and for a longer duration at lower temperatures (Q(10) of 2.29-2.41), consistent with a slowing of its contractile rates. Muscle recruitment was unaffected by temperature, as revealed by the lack of thermal dependence in the intensity of activity of both the jaw depressor and jaw levator muscles (Q(10) of 0.754-1.12). Over the 20-35°C range, lower thermal dependence was found for the dynamics of non-elastic movements and the motor control of both elastic and non-elastic movements, in accord with a plateau of high performance found in other systems.

Reproductive phenotype predicts adult bite-force performance in sex-reversed dragons (Pogona vitticeps).

Sex-related differences in morphology and behavior are well documented, but the relative contributions of genes and environment to these traits are less well understood. Species that undergo sex reversal, such as the central bearded dragon (Pogona vitticeps), offer an opportunity to better understand sexually dimorphic traits because sexual phenotypes can exist on different chromosomal backgrounds. Reproductively female dragons with a discordant sex chromosome complement (sex reversed), at least as juveniles, exhibit traits in common with males (e.g., longer tails and greater boldness). However, the impact of sex reversal on sexually dimorphic traits in adult dragons is unknown. Here, we investigate the effect of sex reversal on bite-force performance, which may be important in resource acquisition (e.g., mates and/or food). We measured body size, head size, and bite force of the three sexual phenotypes in a colony of captive animals. Among adults, we found that males (ZZm) bite more forcefully than either chromosomally concordant females (ZWf) or sex-reversed females (ZZf), and this difference is associated with having relatively larger head dimensions. Therefore, adult sex-reversed females, despite apparently exhibiting male traits as juveniles, do not develop the larger head and enhanced bite force of adult male bearded dragons. This pattern is further illustrated in the full sample by a lack of positive allometry of bite force in sex-reversed females that is observed in males. The results reveal a close association between reproductive phenotype and bite force performance, regardless of sex chromosome complement.

Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards.

We investigate the roles of mitochondrial introgression and incomplete lineage sorting during the phylogenetic history of crotaphytid lizards. Our Bayesian phylogenetic estimate for Crotaphytidae is based on analysis of mitochondrial DNA sequence data for 408 individuals representing the 12 extant species of Crotaphytus and Gambelia. The mitochondrial phylogeny disagrees in several respects with a previously published morphological tree, as well as with conventional species designations, and we conclude that some of this disagreement stems from hybridization-mediated mitochondrial introgression, as well as from incomplete lineage sorting. Unidirectional introgression of Crotaphytus collaris (western collared lizard) mitochondria into C. reticulatus (reticulate collared lizard) populations in the Rio Grande Valley of Texas has resulted in the replacement of ancestral C. reticulatus mitochondria over approximately two-thirds of the total range of the species, a linear distance of approximately 270 km. Introgression of C. collaris mitochondria into C. bicinctores (Great Basin collared lizard) populations in southwestern Arizona requires a more complex scenario because at least three temporally separated and superimposed introgression events appear to have occurred in this region. We propose an "introgression conveyor" model to explain this unique pattern of mitochondrial variation in this region. We show with ecological niche modeling that the predicted geographical ranges of C. collaris, C. bicinctores, and C. reticulatus during glacial maxima could have provided enhanced opportunities for past hybridization. Our analyses suggest that incomplete lineage sorting and/or introgression has further confounded the phylogenetic placements of additional species including C. nebrius, C. vestigium, C. insularis, C. grismeri, and perhaps G. copei. Despite many independent instances of interspecific hybridization among crotaphytid lizards, the species continue to maintain morphological and geographic cohesiveness throughout their ranges.

Bite force in the horned frog (Ceratophrys cranwelli) with implications for extinct giant frogs.

Of the nearly 6,800 extant frog species, most have weak jaws that play only a minor role in prey capture. South American horned frogs (Ceratophrys) are a notable exception. Aggressive and able to consume vertebrates their own size, these "hopping heads" use a vice-like grip of their jaws to restrain and immobilize prey. Using a longitudinal experimental design, we quantified the ontogenetic profile of bite-force performance in post-metamorphic Ceratophrys cranwelli. Regression slopes indicate positive allometric scaling of bite force with reference to head and body size, results that concur with scaling patterns across a diversity of taxa, including fish and amniotes (lizards, tuatara, turtles, crocodylians, rodents). Our recovered scaling relationship suggests that exceptionally large individuals of a congener (C. aurita) and extinct giant frogs (Beelzebufo ampinga, Late Cretaceous of Madagascar) probably could bite with forces of 500 to 2200 N, comparable to medium to large-sized mammalian carnivores.

Gaping displays reveal and amplify a mechanically based index of weapon performance.

Physical prowess, a key determinant of fight outcomes, is contingent on whole-organism performance traits. The advertisement of performance, via display, is poorly understood because it is unclear how information about performance is encoded into display characteristics. Previous studies have shown that weapon performance (i.e., bite force) predicts dominance and reproductive success in male lizards. We tested the hypothesis that gaping displays by adult male collared lizards (Crotaphytus) can provide an index of weapon performance by exposing the major jaw-adductor muscle complex and that white patches at the mouth corners amplify this index. For territorial adult males, the breadth of the muscle complex, which is not correlated with body size, was a strong predictor of bite force. For nonterritorial yearling males and females, however, measures of body and head size predicted bite force. The patches are highly conspicuous, exhibit UV-reflecting properties within the visual range of lizards, and provide size-independent information about bite force only in adult males. We conclude that exposure of the muscle complex during gaping displays can provide rival males with a reliable, body-size independent, biomechanically based index of weapon performance, an index that the mouth-corner patches amplify. Indexes that transmit information through mechanistic links to performance are expected to be widespread among animals.

Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris).

In territorial polygynous taxa, reproductive success reflects phenotypic variation. Using Crotaphytus collaris, a sexually dimorphic lizard in which males use the head (i.e., jaws and associated musculature) as a weapon when territorial interactions escalate to fights, we tested the hypothesis that weapon performance (i.e., bite force) is a better predictor of fitness than body or weapon size. Bite-force performance predicted the number of female home ranges overlapped, estimated mating success, and potential reproductive output. However, no body or weapon size measure correlated with these estimates of fitness, and only one weapon dimension (head width) correlated with bite force. These results indicate that weapon performance has far stronger effects on fitness than body or weapon size, likely because it directly influences fight outcomes. As such, it is desirable that the use of morphology as a proxy for performance and its presumed extensions to fitness be based on empirical morphology-performance relationships.

Feeding behavior modulation in the leopard lizard (Gambelia wislizenii): effects of noxious versus innocuous prey.

Feeding, a fundamentally rhythmic behavior in many animals, is expected to exhibit modulation with respect to prey type. Using high-speed videography (200 frames(-1)) and kinematic analysis, we investigated prey-processing behavior in the long-nosed leopard lizard (Gambelia wislizenii). The effects of two prey types were examined, innocuous immature crickets (Acheta domesticus) and noxious stinging hymenopterans (honeybees [Apis mellifer] and yellow jackets [Vespula sp.]). Stinging hymenopterans are processed more extensively, with higher gape-cycling frequencies, and for a greater duration than are crickets. Generalized tetrapod feeding models were used as a framework to test the hypothesis that gape profile characteristics are modulated in response to prey noxiousness. Cricket processing generally fits the models, but hymenopteran processing departs from typical model parameters. In particular, the SO phase is absent to barely detectable during hymenopteran processing. This likely represents an effect of extrinsic neural input on a centrally directed rhythmic motor pattern, possibly to avoid being stung. Differences in the capture behavior of crickets versus hymenopterans indicate that G. wislizenii assesses prey noxiousness before physical contact with prey and modifies its capture behavior accordingly. These results add to the growing body of evidence that sensory information can play a critical role in shaping stereotyped rhythmic behaviors in non-mammalian tetrapods.

Burst-swimming performance predicts the outcome of cannibalistic interactions in green poison frog larvae (Dendrobates auratus).

Whole-animal performance (e.g., swimming speed, bite force) functions as a fundamental link between organism and environment and, as such, performance characteristics are important in determining the outcomes of agonistic interactions, both interspecific and intraspecific. Cannibalism is an intraspecific agonistic interaction for which winners may be expected to exhibit superior performance in characteristics relevant to cannibalistic behavior. The larvae of the Green Poison Frog (Dendrobates auratus) exhibit cannibalistic behavior in which "fast-starts" (i.e., high velocity and acceleration from a resting position) are used in attempts to bite and avoid being bitten by conspecifics. We tested the hypothesis that superior fast-start swimming performance is positively associated with winning cannibalistic interactions between similarly sized individuals. Fast-starts by larvae were imaged with a high-speed camera, and pairs of size-matched individuals then underwent interaction trials to determine whether swimming performance is associated with winning a cannibalistic interaction. Linear acceleration of the snout tip, approximating the position of the mouthparts used to attack an opponent, was significantly greater in winners than losers. At the estimated center of mass, generally representing a target for an attacking opponent, linear velocity and acceleration were significantly greater in winners than losers. Understanding the role of performance in intraspecific interactions can help elucidate how they contribute to population dynamics, and thus how such interactions ultimately drive morphological and behavioral evolution.

Phenomenological models of the dynamics of muscle during isotonic shortening.

We investigated the effectiveness of simple, Hill-type, phenomenological models of the force-length-velocity relationship for simulating measured length trajectories during muscle shortening, and, if so, what forms of the model are most useful. Using isotonic shortening data from mouse soleus and toad depressor mandibulae muscles, we showed that Hill-type models can indeed simulate the shortening trajectories with sufficiently good accuracy. However, we found that the standard form of the Hill-type muscle model, called the force-scaling model, is not a satisfactory choice. Instead, the results support the use of less frequently used models, the f-max scaling model and force-scaling with parallel spring, to simulate the shortening dynamics of muscle.

Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation.

BACKGROUND: Crocodilians have dominated predatory niches at the water-land interface for over 85 million years. Like their ancestors, living species show substantial variation in their jaw proportions, dental form and body size. These differences are often assumed to reflect anatomical specialization related to feeding and niche occupation, but quantified data are scant. How these factors relate to biomechanical performance during feeding and their relevance to crocodilian evolutionary success are not known. METHODOLOGY/PRINCIPAL FINDINGS: We measured adult bite forces and tooth pressures in all 23 extant crocodilian species and analyzed the results in ecological and phylogenetic contexts. We demonstrate that these reptiles generate the highest bite forces and tooth pressures known for any living animals. Bite forces strongly correlate with body size, and size changes are a major mechanism of feeding evolution in this group. Jaw shape demonstrates surprisingly little correlation to bite force and pressures. Bite forces can now be predicted in fossil crocodilians using the regression equations generated in this research. CONCLUSIONS/SIGNIFICANCE: Critical to crocodilian long-term success was the evolution of a high bite-force generating musculo-skeletal architecture. Once achieved, the relative force capacities of this system went essentially unmodified throughout subsequent diversification. Rampant changes in body size and concurrent changes in bite force served as a mechanism to allow access to differing prey types and sizes. Further access to the diversity of near-shore prey was gained primarily through changes in tooth pressure via the evolution of dental form and distributions of the teeth within the jaws. Rostral proportions changed substantially throughout crocodilian evolution, but not in correspondence with bite forces. The biomechanical and ecological ramifications of such changes need further examination.

Elastic properties of active muscle--on the rebound?

During active lengthening and shortening, muscles exhibit a variety of time-dependent spring properties, including load-dependent and nonlinear stiffness. These properties can be explained as interactions between a spring element and cycling cross bridges within muscle sarcomeres. Several lines of evidence suggest a role for the giant protein titin in active muscle, but specific mechanisms remain to be elucidated.

Neuromechanics: an integrative approach for understanding motor control.

Neuromechanics seeks to understand how muscles, sense organs, motor pattern generators, and brain interact to produce coordinated movement, not only in complex terrain but also when confronted with unexpected perturbations. Applications of neuromechanics include ameliorating human health problems (including prosthesis design and restoration of movement following brain or spinal cord injury), as well as the design, actuation and control of mobile robots. In animals, coordinated movement emerges from the interplay among descending output from the central nervous system, sensory input from body and environment, muscle dynamics, and the emergent dynamics of the whole animal. The inevitable coupling between neural information processing and the emergent mechanical behavior of animals is a central theme of neuromechanics. Fundamentally, motor control involves a series of transformations of information, from brain and spinal cord to muscles to body, and back to brain. The control problem revolves around the specific transfer functions that describe each transformation. The transfer functions depend on the rules of organization and operation that determine the dynamic behavior of each subsystem (i.e., central processing, force generation, emergent dynamics, and sensory processing). In this review, we (1) consider the contributions of muscles, (2) sensory processing, and (3) central networks to motor control, (4) provide examples to illustrate the interplay among brain, muscles, sense organs and the environment in the control of movement, and (5) describe advances in both robotics and neuromechanics that have emerged from application of biological principles in robotic design. Taken together, these studies demonstrate that (1) intrinsic properties of muscle contribute to dynamic stability and control of movement, particularly immediately after perturbations; (2) proprioceptive feedback reinforces these intrinsic self-stabilizing properties of muscle; (3) control systems must contend with inevitable time delays that can simplify or complicate control; and (4) like most animals under a variety of circumstances, some robots use a trial and error process to tune central feedforward control to emergent body dynamics.

Storage and recovery of elastic potential energy powers ballistic prey capture in toads.

Ballistic tongue projection in toads is a remarkably fast and powerful movement. The goals of this study were to: (1) quantify in vivo power output and activity of the depressor mandibulae muscles that are responsible for ballistic mouth opening, which powers tongue projection; (2) quantify the elastic properties of the depressor mandibulae muscles and their series connective tissues using in situ muscle stimulation and force-lever studies; and (3) develop and test an elastic recoil model, based on the observed elastic properties of the depressor mandibulae muscles and series connective tissues, that accounts for displacement, velocity, acceleration and power output during ballistic mouth opening in toads. The results demonstrate that the depressor mandibulae muscles of toads are active for up to 250 ms prior to mouth opening. During this time, strains of up to 21.4% muscle resting length (ML) develop in the muscles and series connective tissues. At maximum isometric force, series connective tissues develop strains up to 14% ML, and the muscle itself develops strains up to 17.5% ML. When the mouth opens rapidly, the peak instantaneous power output of the depressor mandibulae muscles and series connective tissues can reach 9600 W kg(-1). The results suggest that: (1) elastic recoil of muscle itself can contribute significantly to the power of ballistic movements; (2) strain in series elastic elements of the depressor mandibulae muscle is too large to be borne entirely by the cross bridges and the actin-myosin filament lattice; and (3) central nervous control of ballistic tongue projection in toads likely requires the specification of relatively few parameters.