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Dry versus wet and gross: Comparisons between the dry skull method and gross dissection in estimations of jaw muscle cross‐sectional area and bite forces in sea otters
Abstract
Bite force is a measure of feeding performance used to elucidate links between animal morphology, ecology, and fitness. Obtaining live individuals for in vivo bite-force measurements or freshly deceased specimens for bite force modeling is challenging for many species. Thomason's dry skull method for mammals relies solely on osteological specimens and, therefore, presents an advantageous approach that enables researchers to estimate and compare bite forces across extant and even extinct species. However, how accurately the dry skull method estimates physiological cross-sectional area (PCSA) of the jaw adductor muscles and theoretical bite force has rarely been tested. Here, we use an ontogenetic series of southern sea otters (Enhydra lutris nereis) to test the hypothesis that skeletomuscular traits estimated from the dry skull method accurately predicts test traits derived from dissection-based biomechanical modeling. Although variables from these two methods exhibited strong positive relationships across ontogeny, we found that the dry skull method overestimates PCSA of the masseter and underestimates PCSA of the temporalis. Jaw adductor in-levers for both jaw muscles and overall bite force are overestimated. Surprisingly, we reveal that sexual dimorphism in craniomandibular shape affects temporalis PCSA estimations; the dry skull method predicted female temporalis PCSA well but underestimates male temporalis PCSA across ontogeny. These results highlight the importance of accounting for sexual dimorphism and other intraspecific variation when using the dry skull method. Together, we found the dry skull method provides an underestimation of bite force over ontogeny and that the underlying anatomical components driving bite force may be misrepresented.
... Studies of bite force vary widely in methodology, and each methodology comes with its suite of limitations. For example, in vivo measurements of bite force provide direct estimations, but samples are often limited, and working alongside live animals can be dangerous (Herrel et al. 2008;Davis et al. 2010;Law & Mehta 2019); biomechanical modeling with freshly dissected feeding apparatuses can be challenging due to the difficulty of obtaining deceased individuals of wild or rare animals Santana et al. 2010;Hartstone-Rose et al. 2012;Gignac & Erickson 2016). Many mammalogists estimate bite forces using models; the most frequently used is a two-dimensional picture-based technique known as the "dry-skull method" (Thomason 1991). ...
... Many mammalogists estimate bite forces using models; the most frequently used is a two-dimensional picture-based technique known as the "dry-skull method" (Thomason 1991). This method relies on estimated cross-sectional areas of the jaw adductor muscles from photographs of skulls (Law & Mehta 2019;Thomason 1991). Photographs can be easily obtained, as the skulls are often part of museum collections, and can thus be used to study large numbers of extant and extinct species to explore patterns of bite force through time or across large phylogenetic groups (e.g. ...
... For example, chewing performance can be influenced by factors such as muscle fiber type composition (Holmes & Taylor 2021), morphology of dental occlusal surface (Koc et al. 2010), tooth material properties (Herbst et al. 2021), and jaw kinematics during mastication (Kuninori et al. 2014). It is important to take into account that the dry-skull method used in this study has its limitations (Ellis et al. 2008;Law & Mehta 2019;Bates et al. 2021;), including over-or underestimation of muscle physiological cross-sectional area and underestimation of bite force. For comparative purposes, in this study, the method models muscle forces as vertically oriented single force vectors. ...
Bite force is often associated with specific morphological features, such as sagittal crests. The presence of a pronounced sagittal crest in some tapirs (Perissodactyla: Tapiridae) was recently shown to be negatively correlated with hard-object feeding, in contrast with similar cranial structures in carnivorans. The aim of this study was to investigate bite forces and sagittal crest heights across a wide range of modern and extinct tapirs and apply a comparative investigation to establish whether these features are correlated across a broad phylogenetic scope. We examined a sample of 71 specimens representing 15 tapir species (five extant, ten extinct) using the dry-skull method, linear measurements of cranial features, phylogenetic reconstruction, and comparative analyses. Tapirs were found to exhibit variation in bite force and sagittal crest height across their phylogeny and between different biogeographical realms, with high-crested morphologies occurring mostly in Neotropical species. The highest bite forces within tapirs appear to be driven by estimates for the masseter - pterygoid muscle complex, rather than predicted forces for the temporalis muscle. Our results demonstrate that relative sagittal crest height is poorly correlated with relative cranial bite force, suggesting high force application is not a driver for pronounced sagittal crests in this sample. The divergent biomechanical capabilities of different contemporaneous tapirids may have allowed multiple species to occupy overlapping territories and partition resources to avoid excess competition. Bite forces in tapirs peak in Pleistocene species, independent of body size, suggesting possible dietary shifts as a potential result of climatic changes during this epoch. This article is protected by copyright. All rights reserved.
... However, the ability of MAA-based methods to accurately reconstruct qualitative and quantitative functional patterns in a macroevolutionary radiation has not been extensively tested. To date, measures of accuracy have largely been restricted to single taxon studies of muscle anatomy and bite force [1,[29][30][31][32][33][34]. The varying levels of inaccuracy recovered by these studies contrasts somewhat with a single comparative study of bats, which found that the method accurately predicted bite forces despite inaccurately predicting muscle parameters [35]. ...
... MAA-based approaches to estimate muscle size and forcegenerating capacity, and subsequently bone loading, have been widely applied to extinct and extant taxa to examine the functional consequences of changing morphology and macroevolutionary patterns in the locomotor, axial and masticatory systems of vertebrates (e.g. ). Our study of its application to rodent masticatory morphotypes builds upon a small number of previous evaluations of such approaches [1,[29][30][31][32][33][34][35] in a number of ways: by extending assessment to FE models; by providing assessment of qualitative and quantitative accuracy in an explicit macroevolutionary context; and by direct comparison to the most widely used alternative method of numerical soft tissue reconstruction (volume sculpture; e.g. [36][37][38][39][40][41][42]). ...
... [36][37][38][39][40][41][42]). Previous studies that have examined the accuracy of the dry skull method have suggested that the approach overestimates the PCSA of the masseter muscles and medial pterygoid, while underestimating the PCSA of the temporalis [1,[29][30][31]. Here, we find a different pattern of error, possibly owing to our taxonomic focus on rodents compared to that of previous evaluations of the dry skull method, which used opossums, carnivorans and bats. ...
Measures of attachment or accommodation area on the skeleton are a popular means of rapidly generating estimates of muscle proportions and functional performance for use in large-scale macroevolutionary studies. Herein, we provide the first evaluation of the accuracy of these muscle area assessment (MAA) techniques for estimating muscle proportions, force outputs and bone loading in a comparative macroevolutionary context using the rodent masticatory system as a case study. We find that MAA approaches perform poorly, yielding large absolute errors in muscle properties, bite force and particularly bone stress. Perhaps more fundamentally, these methods regularly fail to correctly capture many qualitative differences between rodent morphotypes, particularly in stress patterns in finite-element models. Our findings cast doubts on the validity of these approaches as means to provide input data for biomechanical models applied to understand functional transitions in the fossil record, and perhaps even in taxon-rich statistical models that examine broad-scale macroevolutionary patterns. We suggest that future work should go back to the bones to test if correlations between attachment area and muscle size within homologous muscles across a large number of species yield strong predictive relationships that could be used to deliver more accurate predictions for macroevolutionary and functional studies.
... Care must be taken in comparing the muscle force of Z. californianus to the other species, however, because it was estimated from direct dissections and the dry skull method that was used on the other species is known to underestimate PCSA for the temporalis muscle and to overestimate it for the masseter Sakamoto et al. 2010;Law and Mehta 2019). For the temporalis the discrepancy is small, with dry skull estimates being about 80% of the true value in otters; for the masseter the discrepancy was much larger, but in the opposite direction with most dry skull estimates being larger than they truly are (Law and Mehta 2019). ...
... Care must be taken in comparing the muscle force of Z. californianus to the other species, however, because it was estimated from direct dissections and the dry skull method that was used on the other species is known to underestimate PCSA for the temporalis muscle and to overestimate it for the masseter Sakamoto et al. 2010;Law and Mehta 2019). For the temporalis the discrepancy is small, with dry skull estimates being about 80% of the true value in otters; for the masseter the discrepancy was much larger, but in the opposite direction with most dry skull estimates being larger than they truly are (Law and Mehta 2019). Adjusting our Z. ...
Behavioral foraging differences are known to aid in food resource partitioning in pinniped communities, but it is not known whether skull biomechanical efficiency also contributes to dietary niche partitioning. We tested this hypothesis in a community of four sympatric species of pinnipeds that co-occur along the coast of Baja California: California sea lion (Zalophus californianus), northern elephant seal (Mirounga angustirostris), harbor seal (Phoca vitulina), and Guadalupe fur seal (Arctocephalus townsendi). We tested whether their preferred prey items differed in resistivity to puncture and whether those differences were linked to the mass of the muscles of mastication and the biomechanical efficiency with which they can puncture prey items. For each prey species, we measure resistivity to puncture using texture profile analysis. We found that M. angustirostris consumes the
most resistant prey and that A. townsendi consumes the least resistant. We estimated physiological cross-sectional area of the muscles of mastication for each pinniped and found that the same pair of species respectively has the largest and smallest
theoretical value of muscular force. Finally, we estimated the bite force that each pinniped species requires to puncture its prey by solving Euler-Lagrange equations based on biomechanical lever model parameters measured from 3D digital models of the
skulls.We also found differences in efficiency between the species. These data allowed us to classify the three ecomorphological types. Type 1 features a hydrodynamic skull with relatively low mandibular forces, characteristic of pelagic carnivore feeders
such as A. townsendi. Type 2, represented by Z. californianus and M. angustirostris (both opportunistic feeders), is characterized by broad insertion areas for the mandibular muscles and strong teeth, permitting these predators to vary the prey target species as
a function of prey availability. Type 3 features a less robust skull and a lower muscle efficiency, characteristic of benthic feeders such as P. vitulina. This evidence indicates that biomechanical differences between the species contribute to dietary niche construction.
... We found that the maximal bite forces of the Andean spectacled bears and the lion we recorded are well above those predicted for these species based on the dry skull method (Christiansen, 2007). This underestimation is a known shortcoming of the dry skull method, in part owing to an overestimation of the physiological cross-sectional area (PCSA) of the masseter and underestimation of the PCSA of the temporalis muscle (Law and Mehta, 2019;Thomason, 1991;Wroe et al., 2005). In the case of the Malayan sun bears, when corrected for the mechanical advantage of the rear molar, the in vivo values of 1907-2021 N are within the upper range of the estimated maximal force of 1722±423 N. ...
Bite force is a key performance trait of the feeding system, but maximal in vivo bite force has been measured in few large mammals. The alternative, modelling of bite force from anatomy, cannot be validated without in vivo measurements. To overcome existing limitations of ethics, safety, and animal well-being, we here propose a semi-automated method to obtain voluntary maximum bite forces from large mammals using bite plates that automatically dispense a food reward if an incrementally increasing threshold force value is reached. We validated our method using two Malayan sun bears, two Andean spectacled bears and a lioness. We show that voluntary bite force measurement using positive reinforcement is a non-invasive and reliable method to record maximum voluntary bite force performance in large mammals. Our results further show that in vivo data are critical as modeling efforts from osteology have greatly underestimated bite forces in Andean bears.
... Thomason (1991: his figure 3) found strong correlation between carnivoran jaw muscle PCSAs used to estimate forces, and the projected area of the temporal fossa-a proxy for AA widely used in the 'dry skull method'. Law and Mehta (2019) also uncovered similar correlations for sea otters using the dry skull method, although they cautioned that different muscles have rather different correlations, and sexual dimorphism as well as ontogeny complicate these correlations. Antón (2000), however, found that macaque species have varying allometries of pterygoid jaw muscles and overall noisy correlations between PCSAs and AA (or origin-insertion distances: see their figure 4), expressing scepticism that PCSA estimation from AA could reliably be conducted with fossil primates. ...
In vertebrates, active movement is driven by muscle forces acting on bones, either directly or through tendinous insertions. There has been much debate over how muscle size and force are reflected by the muscular attachment areas (AAs). Here we investigate the relationship between the physiological cross-sectional area (PCSA), a proxy for the force production of the muscle, and the AA of hindlimb muscles in Nile crocodiles and five bird species. The limbs were held in a fixed position whilst blunt dissection was carried out to isolate the individual muscles. AAs were digitised using a point digitiser, before the muscle was removed from the bone. Muscles were then further dissected and fibre architecture was measured, and PCSA calculated. The raw measures, as well as the ratio of PCSA to AA, were studied and compared for intra-observer error as well as intra- and interspecies differences. We found large variations in the ratio between AAs and PCSA both within and across species, but muscle fascicle lengths are conserved within individual species, whether this was Nile crocodiles or tinamou. Whilst a discriminant analysis was able to separate crocodylian and avian muscle data, the ratios for AA to cross-sectional area for all species and most muscles can be represented by a single equation. The remaining muscles have specific equations to represent their scaling, but equations often have a relatively high success at predicting the ratio of muscle AA to PCSA. We then digitised the muscle AAs of Coelophysis bauri, a dinosaur, to estimate the PCSAs and therefore maximal isometric muscle forces. The results are somewhat consistent with other methods for estimating force production, and suggest that, at least for some archosaurian muscles, that it is possible to use muscle AA to estimate muscle sizes. This method is complementary to other methods such as digital volumetric modelling.
Background
An ontogenetic niche shift in vertebrates is a common occurrence where ecology shifts with morphological changes throughout growth. How ecology shifts over a vertebrate’s lifetime is often reconstructed in extant species—by combining observational and skeletal data from growth series of the same species—because interactions between organisms and their environment can be observed directly. However, reconstructing shifts using extinct vertebrates is difficult and requires well-sampled growth series, specimens with relatively complete preservation, and easily observable skeletal traits associated with ecologies suspected to change throughout growth, such as diet.
Methods
To reconstruct ecological changes throughout the growth of a stem-mammal, we describe changes associated with dietary ecology in a growth series of crania of the large-bodied (∼2 m in length) and herbivorous form, Exaeretodon argentinus (Cynodontia: Traversodontidae) from the Late Triassic Ischigualasto Formation, San Juan, Argentina. Nearly all specimens were deformed by taphonomic processes, so we reconstructed allometric slope using a generalized linear mixed effects model with distortion as a random effect.
Results
Under a mixed effects model, we find that throughout growth, E. argentinus reduced the relative length of the palate, postcanine series, orbits, and basicranium, and expanded the relative length of the temporal region and the height of the zygomatic arch. The allometric relationship between the zygomatic arch and temporal region with the total length of the skull approximate the rate of growth for feeding musculature. Based on a higher allometric slope, the zygoma height is growing relatively faster than the length of the temporal region. The higher rate of change in the zygoma may suggest that smaller individuals had a crushing-dominated feeding style that transitioned into a chewing-dominated feeding style in larger individuals, suggesting a dietary shift from possible faunivory to a more plant-dominated diet. Dietary differentiation throughout development is further supported by an increase in sutural complexity and a shift in the orientation of microwear anisotropy between small and large individuals of E. argentinus . A developmental transition in the feeding ecology of E. argentinus is reflective of the reconstructed dietary transition across Gomphodontia, wherein the earliest-diverging species are inferred as omnivorous and the well-nested traversodontids are inferred as herbivorous, potentially suggesting that faunivory in immature individuals of the herbivorous Traversodontidae may be plesiomorphic for the clade.
Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size‐corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in it's entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size‐corrected estimated bite force. Many‐to‐one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size‐corrected bite force evolution. While musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially non‐feeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviors reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial, and appendicular form and function with behavioral observations will reveal further insights in the evolution of dietary ecologies and other ecological variables.
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Analyses of masticatory muscle architecture—specifically fascicle length (FL; a correlate of muscle stretch and contraction speed) and physiological cross-sectional area (PCSA; a correlate of force)—reveal soft-tissue dietary adaptations. For instance, consumers of large, soft foods are expected to have relatively long FL, while consumers of obdurate foods are expected to have relatively high PCSA. Unfortunately, only a few studies have analyzed these variables across large primate samples—an order of particular interest because it is our own. Previous studies found that, in strepsirrhines, force variables (PCSA and muscle masses; MM) scale with isometry or slight positive allometry, while the body size corrected FL residuals correlate with food sizes. However, a study of platyrrhines using different methods (in which the authors physically cut muscles between fascicles) found very different trends: negative allometry for both the stretch and force variables. Here, we apply the methods used in the strepsirrhine study (chemical dissection of fascicles to ensure full length measurements) to reevaluate these trends in platyrrhines and extend this research to include catarrhines. Our results conform to the previous strepsirrhine trends: there is no evidence of negative allometry in platyrrhines. Rather, in primates broadly and catarrhines specifically, MM and PCSA scale with isometry or positive allometry. When examining size-adjusted variables, it is clear that fascicle lengths (especially those of the temporalis muscle) correlate with diet: species that consume soft, larger, foods have longer masticatory fiber lengths which would allow them to open their jaws to wider gape angles. Anat Rec, 301:311–324, 2018. © 2018 Wiley Periodicals, Inc.
This issue of the Anatomical Record is the first of a two-volume set that focuses on new investigations into behavioral correlates of muscle functional morphology. Much of the research on functional morphology and adaptation to specific functional niches focuses on the shapes of hard-tissues—bones and teeth. Investigations into soft-tissue anatomy tend to be predominantly descriptive with only brief allusion to ontogenetic or evolutionary origins of structures. When muscles are included in analyses of functional systems, their function tends to be oversimplified—usually considered a simple force vector connecting two osteological points, with the force treated as a constant derived from some simple calculation of muscle size. The goal of these special issues is to present a series of studies that take a more elaborate look at how muscles can be viewed from a functional perspective in studies searching for morphological correlates of behavior. This first volume focuses on the behavioral correlates of cranial muscles—starting with a paper about the mimetic musculature of primates and ending with a series of papers on the masticatory muscles of many lineages of vertebrates. The next issue of the Anatomical Record (March 2018) includes our papers on the behavioral correlates of postcranial muscles. Taken together, we hope you agree that this series presents valuable insights into these form/function relationships using both traditional approaches+ and cutting-edge techniques. Anat Rec, 301:197–201, 2018. © 2018 Wiley Periodicals, Inc.
Weaning represents a major ontogenetic dietary shift in southern sea otters (Enhydra lutris nereis), as juveniles must transition from depending on mother’s milk to independently processing hard-shelled invertebrates. When the skulls of juveniles have reached sufficient maturity to transition to a durophagous diet remains to be investigated. Here, we conducted a comprehensive analysis of skull development and growth and sexual dimorphism using geometric morphometric approaches in 204 southern sea otter skulls. We found that southern sea otters of both sexes exhibit dramatic changes in cranial and mandibular shape and size over ontogeny. Although the majority of these changes occur in the pup stage, full development and growth of the skull does not occur until well after weaning. We hypothesize that the slower maturation of the crania of newly weaned juveniles serves as a handicap by constraining jaw adductor muscle size, biting ability and feeding on hard-shelled prey. In our analysis of sexual dimorphism, we found significant sexual shape and size dimorphism in adult craniomandibular morphology that arose through differences in developmental and growth rates and duration. We postulate that males are selected to attain mature crania faster to presumably reach adult biting ability sooner, gaining a competitive advantage in obtaining food and in male–male agonistic interactions.
The niche divergence hypothesis suggests that if a species exhibits intersexual differences in diet, selection should favor divergence in the feeding apparatus between the sexes. Recent work revealed that male and female southern sea otters (Enhydra lutris nereis) utilize different dietary resources in response to increased population density; females exhibit more specialized diets as a function of smaller home ranges, whereas males exhibit larger home ranges, potentially allowing them to expand their dietary breadths by feeding on prey items that are not found in female home ranges. These dietary differences suggest the potential for sexual dimorphism of the feeding apparatus (i.e., the skull). Here, we tested the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits directly related to biting ability. Univariate and multivariate analyses of 12 craniomandibular traits showed that size is the primary axis of skull variation, whereas only a handful of craniomandibular traits demonstrated significant shape differences between the sexes. Relative postorbital constriction breadth, masseter in-lever length, and cranial height differed significantly between the sexes. These 3 traits can increase the surface area of jaw muscle attachment sites and thus are directly linked to the mechanics of biting ability. Collectively, these morphological differences indicate that niche divergence may be an important mechanism maintaining sexual dimorphism in southern sea otters.
Sexual dimorphism attributed to niche divergence is often linked to differentiation between the sexes in both dietary resources and characters related to feeding and resource procurement. Although recent studies have indicated that southern sea otters (Enhydra lutris nereis) exhibit differences in dietary preferences as well as sexual dimorphism in skull size and shape, whether these intersexual differences translate to differentiation in feeding performances between the sexes remains to be investigated. To test the hypothesis that scaling patterns of bite force, a metric of feeding performance, differ between the sexes, we calculated theoretical bite forces for 55 naturally deceased male and female southern sea otters spanning the size ranges encountered over ontogeny. We then used standardized major axis regressions to simultaneously determine the scaling patterns of theoretical bite forces and skull components across ontogeny and assess whether these scaling patterns differed between the sexes. We found that positive allometric increases in theoretical bite force resulted from positive allometric increases in physiological cross-sectional area for the major jaw adductor muscle and mechanical advantage. Closer examination revealed that allometric increases in temporalis muscle mass and relative allometric decreases in out-lever lengths are driving these patterns. In our analysis of sexual di- morphism, we found that scaling patterns of theoretical bite force and morphological traits do not differ between the sexes. How- ever, adult sea otters differed in their absolute bite forces, revealing that adult males exhibited greater bite forces as a result of their larger sizes. We found intersexual differences in biting ability that provide some support for the niche divergence hypothesis. Continued work in this field may link intersexual differences in feeding functional morphology with foraging ecology to show how niche divergence has the potential to reinforce sexual dimorphism in southern sea otters.
Morphologists have historically had to rely on destructive procedures to visualize the three-dimensional (3-D) anatomy of animals. More recently, however, non-destructive techniques have come to the forefront. These include X-ray computed tomography (CT), which has been used most commonly to examine the mineralized, hard-tissue anatomy of living and fossil metazoans. One relatively new and potentially transformative aspect of current CT-based research is the use of chemical agents to render visible, and differentiate between, soft-tissue structures in X-ray images. Specifically, iodine has emerged as one of the most widely used of these contrast agents among animal morphologists due to its ease of handling, cost effectiveness, and differential affinities for major types of soft tissues. The rapid adoption of iodine-based contrast agents has resulted in a proliferation of distinct specimen preparations and scanning parameter choices, as well as an increasing variety of imaging hardware and software preferences. Here we provide a critical review of the recent contributions to iodine-based, contrast-enhanced CT research to enable researchers just beginning to employ contrast enhancement to make sense of this complex new landscape of methodologies. We provide a detailed summary of recent case studies, assess factors that govern success at each step of the specimen storage, preparation, and imaging processes, and make recommendations for standardizing both techniques and reporting practices. Finally, we discuss potential cutting-edge applications of diffusible iodine-based contrast-enhanced computed tomography (diceCT) and the issues that must still be overcome to facilitate the broader adoption of diceCT going forward.
Variation in terrestrial mammalian skull morphology is known to constrain feeding performance, which in turn influences dietary habits and ultimately fitness. Among mustelids, otters have evolved two feeding specializations: underwater raptorial capture of prey (mouth-oriented) and capture of prey by hand (hand-oriented), both of which have likely associations with morphology and bite performance. However, feeding biomechanics and performance data for otters are sparse. The first goal of this study was to investigate the relationships between feeding morphology and bite performance among two mouth-oriented piscivores (Pteronura brasiliensis and Lontra canadensis) and two hand-oriented invertebrate specialists (Enhydra lutris and Aonyx cinerea). Since other vertebrate taxa that are mouth-oriented piscivores tend to possess longer skulls and mandibles, with jaws designed for increased velocity at the expense of biting capability, we hypothesized that mouth-oriented otters would also possess long, narrow skulls indicative of high velocity jaws. Conversely, hand-oriented otters were expected to possess short, blunt skulls with adaptations to increase bite force and crushing capability. Concomitant with these skull shapes we hypothesized that sea otters would possess a greater mandibular bluntness index, providing for a greater mechanical advantage compared to other otter species investigated. A second goal was to examine morphological variation at a finer scale by assessing variation in cranial morphology among three sea otter subspecies. Since diet varies among these subspecies, and their populations are isolated, we hypothesized that the magnitude of mandibular bluntness and concomitant mechanical advantage, as well as occlusal surface area would also vary within species according to their primary food source (fish versus hard invertebrates). Functional expectations were met for comparisons among and within species. Among species the phylogeny suggests a deeply rooted transition to alternative foraging types. Yet within foraging types alternative species were also strongly variable, suggesting either selective differences in the extent or nature of realized foraging mode, or an accumulation of non-adaptive changes during the long independent evolutionary history. At the finest scale, variation among subspecies indicates that trophic adaptation occurred rapidly, making it interesting that we happened to find both deeply and shallowly-rooted transformations associated with diet type in otter species and subspecies.
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 critical to testing and evaluating biomechanical models. We reviewed nearly one-hundred 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, as compared to 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 usually is underestimated without standardization because it is expected to be greatest at the minimum out-lever (i.e. back of jaws), which in studies is rarely targeted with success. We assert that future studies should use a pliable substrate, such as leather, and employ appropriate standardization for bite out-lever.
Mammals have developed sophisticated strategies adapting to particular locomotor modes, feeding habits, and social interactions. Many rodent species have acquired a fossorial, semi-fossorial, or even subterranean life-style, converging on morphological, anatomical, and ecological features but diverging in the final arrangement. These ecological variations partially depend on the functional morphology of their digging tools. Muscular and mechanical features (e.g., lever arms relationship) of the bite force were analyzed in three caviomorph rodents with similar body size but different habits and ecological demands of the jaws. In vivo forces were measured at incisors' tip using a strain gauge load cell force transducer whereas theoretical maximal performance values, mechanical advantages, and particular contribution of each adductor muscle were estimated from dissections in specimens of Ctenomys australis (subterranean, solitary), Octodon degus (semi-fossorial, social), and Chinchilla laniger (ground-dweller, colonial). Our results showed that C. australis bites stronger than expected given its small size and C. laniger exhibited the opposite outcome, while O. degus is close to the expected value based on mammalian bite force versus body mass regressions; what might be associated to the chisel-tooth digging behavior and social interactions. Our key finding was that no matter how diverse these rodents' skulls were, no difference was found in the mechanical advantage of the main adductor muscles. Therefore, interspecific differences in the bite force might be primarily due to differences in the muscular development and force, as shown for the subterranean, solitary and territorial C. australis versus the more gracile, ground-dweller, and colonial C. laniger. J. Exp. Zool. 9999A: XX-XX, 2014. © 2014 Wiley Periodicals, Inc.
The mammalian skull has proven to be remarkably plastic during ontogeny and phylogeny in response to the demands of mastication. I examine whether the bending strength of the skull in some mammals correlates with the maximal loads imposed through the masticatory apparatus. The approach is analytical, using the methods of beam theory. Cranial strength is estimated from the second moment of area and other geometrical measurements made from 20–30 transverse CT scans through the skulls of 20 opossums (Didelphis virginiana), and through single skulls of five felid and five canid genera of different sizes. Maximal biting forces were first estimated from areas on the dried skulls bounding the spaces filled in life by the jaw-adducting muscles. These estimates were then adjusted with reference to forces recorded in vivo or, for other specimens, to estimates based on dissections of the jaw muscles. Stress distribution in the face, and peak stresses, were calculated for each animal. Stress levels are low (5–35 MPa) compared with peak stresses in limb bones (40–100 MPa), which correlates with the lower in vivo strains in cranial bones reported in the literature. Stress estimates are in a range that is plausible, which supports the validity of the procedure. Patterns of stress distribution along the face are comparable within each group of animals. Peak stress is independent of size for the carnivorans, but decreases with increasing skull length in D. virginiana. High bending strength of the skull is a consequence of cranial form in mammals; having to enclose the brain, for example, increases the bending strength of the skull. Furthermore, factors such as stiffness or shear and torsional strength may be more important than bending strength. However, bending stress levels appear to be closely regulated, as in other bones that have been studied. The threshold for optimising bending strength and weight is simply at a different level.
Bite force is a measure of whole-organism performance that is often used to investigate the relationships between performance, morphology and fitness. When in vivo measurements of bite force are unavailable, researchers often turn to lever models to predict bite forces. This study demonstrates that bite force predictions based on two-dimensional (2-D) lever models can be improved by including three-dimensional (3-D) geometry and realistic physiological cross-sectional areas derived from dissections. Widely used, the 2-D method does a reasonable job of predicting bite force. However, it does so by over predicting physiological cross-sectional areas for the masseter and pterygoid muscles and under predicting physiological cross-sectional areas for the temporalis muscle. We found that lever models that include the three dimensional structure of the skull and mandible and physiological cross-sectional areas calculated from dissected muscles provide the best predictions of bite force. Models that accurately represent the biting mechanics strengthen our understanding of which variables are functionally relevant and how they are relevant to feeding performance.
American mink are highly sexually dimorphic, with males being up to twice the size of females. Sexual dimorphism may arise for several reasons, including intra- or inter-sexual selection, inter-sexual competition, or divergent reproductive roles. Whether or not dimorphism arises from competition, a degree of niche separation is expected in dimorphic species. Sexual divergence in feeding niche has been reported for many species, including mink. This is likely to be manifested in a greater degree of dimorphism in those structures, such as teeth, that are used for the acquisition of prey. We tested the hypothesis that teeth and other trophic structures of male mink would be significantly larger than those of females, after controlling for underlying skeletal size differences. Canine and carnassial teeth, and several skull dimensions, were larger than predicted in males. There is good evidence that sexual dimorphism in mink trophic apparati is greater than predicted from allometry. We examined the development of dimorphism in various features with age and found that it was not consistent. Several trophic features were dimorphic amongst juveniles, and the degree of dimorphism remained relatively constant with age. Dimorphism in canines, and in relative body mass, was less apparent amongst juveniles and increased with increasing age. We discuss our results in the light of contemporary theories on the evolution and maintenance of sexual size dimorphism and argue that niche separation as a result of dimorphism in trophic features, while probably not the driving force behind sexual size dimorphism, may play a role in its maintenance.
For the past 25 years NIH Image and ImageJ software have been pioneers as open tools for the
analysis of scientific images. We discuss the origins, challenges and solutions of these two programs,
and how their history can serve to advise and inform other software projects.
Summary 1. Relationships between morphology, bite force capacity, prey handling efficiency and trophic niche were explored in two sympatric species of lacertid lizards, Podarcis melisellensis (Braun 1877) and Lacerta oxycephala Duméril & Bibron 1839. 2. Head shape showed little variation, but head size (absolute and relative to snout- vent length, SVL) differed between species and sexes. Males have larger heads than females, both absolute and relative to their SVL. In absolute terms, male P. melisellensis have larger heads than male L. oxycephala , but the reverse case was true for the females. Relative to SVL, L. oxycephala have larger heads than P. melisellensis . 3. Bite force capacity was estimated by having the lizards bite on two metal plates, con- nected to a piezoelectric force transducer. Differences in maximal bite force between species and sexes paralleled differences in absolute head size. Differences in body size and head size explain the higher bite force of males (compared with females), but not the higher bite force of P. melisellensis (compared with L. oxycephala ). Among individual lizards, bite force correlated with body size and head size. 4. Prey handling efficiency, estimated by the time and number of bites needed to subdue a cricket in experimental conditions, also showed intersexual and interspecific vari- ation. This variation corresponded to the differences in maximal bite capacity, suggest- ing that bite force is a determining factor in prey handling. Among individual lizards, both estimates of handling efficiency correlated with maximal bite force capacity. 5. Faecal pellet analyses suggested that in field conditions, males of both sexes select larger and harder prey than females. There was no difference between the species. The proportion of hard-bodied and large-sized prey items found in a lizard's faeces corre- lated positively with its bite force capacity. 6. It is concluded that differences in head and body size, through their effect on bite force capacity, may affect prey selection, either directly, or via handling efficiency.
Bite strength is of great importance to carnivores, as their jaws must produce forces of sufficient magnitude to kill and consume their prey. Spotted hyenas, well known for crushing and consuming bones, were studied to determine how tooth and jaw growth affect bite strength and feeding behaviour. Nine captive individuals, aged 6 months to 2 years of age, were sampled as they grew. At 8- to12-week intervals, morphological measurements that estimated jaw muscle mass, tooth size and skull size were taken. Using a force transducer, bite force was measured directly for these juveniles as well as other captive individuals of different ages. In addition, feeding behaviour and performance were quantified periodically by bone tests in which individuals were offered a sheep femur for 15 min. Behaviour and performance were expected to change with the shift from juvenile to adult dentition. Results were not entirely as expected. Morphological measurements of growth reached a plateau at about 20 months, whereas bite strength increased in a linear fashion up to 5 years of age. A fundamental change in tooth use during bone cracking followed the replacement of deciduous teeth with permanent teeth; the primary area of tooth use moved from anterior to rearmost premolars, increasing the mechanical advantage of the jaw adductors. The timing of this shift seemed to be a function of a decrease in gape limitation as a result of growth as well as caudal movement of the premolars. Our data demonstrated that juvenile hyenas had not achieved adult feeding performance levels at 12 months of age, when they are typically weaned in the wild. This suggests that recently weaned cubs may be at an increased risk of starvation and that selection might favour later weaning times.
1. Two often cited hypotheses explaining sexual head size dimorphism in lizards are: sexual selection acting on structures important in intrasexual competition, and reduction of intersexual competition through food niche separation.
2. In this study some implicit assumptions of the latter hypothesis were tested, namely that an increase in gape distance and bite force should accompany the observed increase in head size. These assumptions are tested by recording bite forces, in vivo , for lizards of the species Gallotia galloti . In this species, male lizards have significantly larger heads than female conspecifics of similar snout–vent length.
3. Additionally, the average force needed to crush several potential prey species was determined experimentally and compared with the bite force data. This comparison clearly illustrates that animals of both sexes can bite much harder than required for most insect food items, which does not support the niche divergence hypothesis. The apparent ‘excess’ bite force in both sexes might be related to the partially herbivorous diet of the animals.
4. To unravel the origin of differences between sexes in bite capacity, the crushing phase of biting was modelled. The results of this model show different strategies in allocation of muscle tissue between both sexes. The origin of this difference is discussed and a possible evolutionary pathway of the development of the sexual dimorphism in the species is provided.
The Common Chuckwalla [Sauromalus ater (= obesus)] is a large, sexually dimorphic lizard with a flattened head that takes refuge from predators in rock crevices. Males use their relatively large heads to bite competing males during territorial fights and to restrain females during copulation. Flattened heads with an antipredator function (i.e. seeking refuge in crevices) and enlarged heads with intrasexual competition and reproductive functions suggest possible antagonism between selective pressures on head morphology in males. To examine this hypothesis, we performed a morphometric analysis and measured the bite-force performance of 49 adult chuckwallas. Males had disproportionately wider heads than females, but did not have deeper heads. Males bit with nearly four times the force of females, consistent with the notion of sexual selection for high bite force in males. Although constrained by crevice-wedging behaviour, head depth was a good predictor of bite force in both sexes. In males, however, osteological head width also was a good predictor of bite force. These results are consistent with the hypothesis that head shape in males is under antagonistic selective pressures, which may partly explain the pattern of head shape dimorphism. The disproportionately wide head of males may reflect anatomical modifications to enhance bite force in response to sexual selection in spite of presumed constraints on head shape for crevice-wedging behaviour © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 215–222.
Measurements of whole-organism performance traits have been useful in studies of adaptation and phenotype–environment correlations. Bite force capacities may be tightly linked to both the type and magnitude of the ecological challenges of food acquisition, mate acquisition, and antipredation in vertebrates. In the present study, we present technical details on bite meters and on measuring bite forces. The ability to take reliable measurements depends on specific features of the measuring device and on where in the mouth the bite is applied. Using both previously available and original data, we demonstrate several ecologically and evolutionarily relevant features of bite force measurements. First, maximal bite forces are repeatable among individuals across all vertebrates studied to date. Second, in ectotherms such as lizards, maximal bite forces are affected by body temperature and motivational states. Third, bite forces are strongly correlated with head size and shape. Fourth, bite forces correlate with features of prey of vertebrates. Finally, bite forces are linked to male dominance and correlated with social-display structures. Thus, bite force performance measures can be used as ‘traits’, and thus be used in integrative studies at multiple levels of organismal biology. Accordingly, bite force data will help our understanding of the functions, capacities, and evolution of jaw–cranial musculoskeletal systems. Moreover, a plethora of opportunities exist for the use of bite force measurements, and if methods are carefully applied, several levels of organismal and ecological organization can be integrated to aid our understanding of the ecology and evolution of vertebrate taxa. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 93, 709–720.
Increasingly, analyses of craniodental dietary adaptations take into account mechanical properties of foods. However, masticatory muscle fiber architecture has been described for relatively few lineages, even though an understanding of the scaling of this anatomy can yield important information about adaptations for stretch and strength in the masticatory system. Data on the mandibular adductors of 28 specimens from nine species of felids representing nearly the entire body size range of the family allow us to evaluate the influence of body size and diet on the masticatory apparatus within this lineage. Masticatory muscle masses scale isometrically, tending toward positive allometry, with body mass and jaw length. This allometry becomes significant when the independent variable is a geometric mean of cranial variables. For all three body size proxies, the physiological cross-sectional area and predicted bite forces scale with significant positive allometry. Average fiber lengths (FL) tend toward negative allometry though with wide confidence intervals resulting from substantial scatter. We believe that these FL residuals are affected by dietary signals within the sample; though the mechanical properties of felid diets are relatively similar across species, the most durophagous species in our sample (the jaguar) appears to have relatively higher force production capabilities. The more notable dietary trend in our sample is the relationship between FL and relative prey size: felid species that predominantly consume relatively small prey have short masticatory muscle fibers, and species that regularly consume relatively large prey have relatively long fibers. This suggests an adaptive signal related to gape.
Morphometric variation in 22 characters of 86 skulls of the European minkMustela lutreola (Linnaeus, 1761), from the NW part of Russia, has been analysed. Stepwise discriminant analysis was used to estimate craniometric variables for sex determinations. Two characters (zygomatic breadth and interorbital width) are enough for the 96.5% correct classification. The male skull ofM. lutreola is characterised by a relatively high neurocranium, widely arranged zygomatic arches, a wide rostrum, and by wider auditory bullae and higher mandibles. Sexual size dimorphism ofM. lutreola is less than that of other similar-sized mustelids —Mustela putorius, M. eversmanii, M. sibirica, Neovison vison. The results are discussed in relation to the existing theories on sexual dimorphism in mustelids.
The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses – the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferroni-type procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.
Differential scaling of musculoskeletal traits leads to differences in performance across ontogeny and ultimately determines patterns of resource use during development. Because musculoskeletal growth of the feeding system facilitates high bite-force generation necessary to overcome the physical constraints of consuming more durable prey, durophagous taxa are well suited for investigations of the scaling relationships between musculoskeletal growth, bite-force generation and dietary ontogeny. To elucidate which biomechanical factors are responsible for allometric changes in bite force and durophagy, we developed and experimentally tested a static model of bite-force generation throughout development in the durophagous turtle Sternotherus minor. Moreover, we quantified the fracture properties of snails found in the diet to evaluate the relationship between bite force and the forces required to process durable prey. We found that (1) the static bite-force model accurately predicts the ontogenetic scaling of bite forces, (2) bite-force positive allometry is accomplished by augmenting muscle size and muscle pennation, and (3) the rupture forces of snails found in the diet show a similar scaling pattern to bite force across ontogeny. These results indicate the importance of muscle pennation for generating high bite forces while maintaining muscle size and provide empirical evidence that the allometric patterns of musculoskeletal growth in S. minor are strongly linked to the structural properties of their primary prey.
Selection can be measured in natural populations by the changes it causes in the means, variances and covariances of phenotypic characters. Furthermore the force of selection can be measured in conventional statistical terms that also play a key role in theoretical equations for evolutionary change. The problem of measuring selection on morphological traits is simplified by breaking the task into two parts: measurement of the effects of morphological variation on performance and measurement of the effects of performance on fitness. The first part can be pursued in the laboratory but the second part is best accomplished in the field. The approach is illustrated with a hypothetical analysis of selection acting on the complex trophic morphology of snakes.
Comparative, functional, and developmental studies of animal morphology require accurate visualization of three-dimensional structures, but few widely applicable methods exist for non-destructive whole-volume imaging of animal tissues. Quantitative studies in particular require accurately aligned and calibrated volume images of animal structures. X-ray microtomography (microCT) has the potential to produce quantitative 3D images of small biological samples, but its widespread use for non-mineralized tissues has been limited by the low x-ray contrast of soft tissues. Although osmium staining and a few other techniques have been used for contrast enhancement, generally useful methods for microCT imaging for comparative morphology are still lacking.
Several very simple and versatile staining methods are presented for microCT imaging of animal soft tissues, along with advice on tissue fixation and sample preparation. The stains, based on inorganic iodine and phosphotungstic acid, are easier to handle and much less toxic than osmium, and they produce high-contrast x-ray images of a wide variety of soft tissues. The breadth of possible applications is illustrated with a few microCT images of model and non-model animals, including volume and section images of vertebrates, embryos, insects, and other invertebrates. Each image dataset contains x-ray absorbance values for every point in the imaged volume, and objects as small as individual muscle fibers and single blood cells can be resolved in their original locations and orientations within the sample.
With very simple contrast staining, microCT imaging can produce quantitative, high-resolution, high-contrast volume images of animal soft tissues, without destroying the specimens and with possibilities of combining with other preparation and imaging methods. Such images are expected to be useful in comparative, developmental, functional, and quantitative studies of morphology.
The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses — the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferronitype procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.
Crocodylians undergo substantial increases in size during ontogeny. The American alligator, Alligator mississippiensis, in particular traverses nearly four orders of body mass between hatching and senescence. Accompanying such changes are modifications in rostrodental morphology and feeding capabilities that facilitate major shifts in diet. How such anatomical changes relate to ecological niche occupation across sizes is not well understood. In this study, we focused on the effects of ontogenetic changes on the force-generating mechanisms for jaw closure to assess the impacts of scaling on feeding biomechanics. We developed dissection-based, musculoskeletal models of maximum bite-force generation throughout ontogeny and compared and tested their veracity with data from an A. mississippiensis developmental series, for which bite forces were directly measured. Through examinations of the scaling patterns within the parameters of our models, we discuss how muscle pennation and positive allometry in the American alligator jaw adductor system facilitate capture strategies and oral processing of prey, and contribute to developmental niche shifts in this large-bodied taxon. On the basis of conservation of the crocodylian jaw adductor system, we argue that our findings are broadly applicable to crown Crocodylia and reflect an important, but often overlooked, aspect of the crocodylian feeding ecomorphology: littoral, sit-and-wait predation is enhanced by posteroventrally displaced, exceptionally large, and forceful ventral pterygoideus muscles, in particular. Future studies on the ontogeny and evolution of feeding in crocodylians should not neglect the functional and ecological implications of these muscles' contributions to diet.
Fifteen variables, selected primarily to reflect functionally significant aspects of cranial morphology, were measured on one skull each of 62 species of modern carnivores, including viverrids, canids, mustelids and felids. To allow comparisons between species of different sizes without the potentially confounding effects of allometric shape changes, the measurements were transformed to dimmensionless variables, based on the residuals from allometric equations. Fourteen out of 15 of the transformed variables distinguish one or more of the four family groups and the rotated first two axes of a principal components analysis distinguish all four families from each other. The following functional hypotheses are proposed: mustelids and felids have the most powerful bites and canids the weakest among the four family groups studied; mustelids and, to a lesser degree, felids have more powerful neck musculature than do canids and viverrids; and visual abilities are best developed among felids and least developed among mustelids. The first two functional hypotheses suggest possible differences in killing behaviour, which are supported by a preliminary survey of the literature on such behaviour. Allometric analysis of the 15 cranial measures shows that the neurocranial components scale with negative allometry, while most of the other measures scale approximately isometrically.
Growth affects the performance of structure, so the pattern of growth must influence the role of a structure and an organism. Because animal performance is linked to morphological specialization, ontogenetic change in size may influence an organism's biological role. High bite force generation is presumably selected for in durophagous taxa. Therefore, these animals provide an excellent study system for investigating biomechanical consequences of growth on performance. An ontogenetic series of 27 cownose rays (Rhinoptera bonasus) were dissected in order to develop a biomechanical model of the feeding mechanism, which was then compared with bite forces measured from live rays. Mechanical advantage of the feeding apparatus was generally conserved throughout ontogeny, while an increase in the mass and cross-sectional area of the jaw adductors resulted in allometric gains in bite force generation. Of primary importance to forceful biting in this taxon is the use of a fibrocartilaginous tendon associated with the insertion of the primary jaw adductor division. This tendon may serve to redirect muscle forces anteriorly, transmitting them within the plane of biting. Measured bite forces obtained through electrostimulation of the jaw adductors in live rays were higher than predicted, possibly due to differences in specific tension of actual batoid muscle and that used in the model. Mass-specific bite forces in these rays are the highest recorded for elasmobranchs. Cownose rays exemplify a species that, through allometric growth of bite performance and morphological novelties, have expanded their ecological performance over ontogeny.
© 2015 Anatomical Society.
An analysis of the masticatory apparatus of three mustelids (Martes, Lutra, Enhydra) is presented. Descriptions are provided for dentition, cranial morphology, primary jaw musculature, and jaw mechanics. The most striking differences noted among the three genera are in the dentition, with the cheek teeth showing extreme modification toward grinding in the species examined. The cranium, jaw muscles, and jaw mechanics are more conservative. These results lend support to the hypothesis that the greatest variation in the components of the mammalian jaw apparatus is contributed by the shape of the teeth (Hiiemae, 1978).
1. The Standardised Major Axis Tests and Routines (SMATR) software provides tools for estimation and inference about allometric lines, currently widely used in ecology and evolution.
2. This paper describes some significant improvements to the functionality of the package, now available on R in smatr version 3.
3. New inclusions in the package include sma and ma functions that accept formula input and perform the key inference tasks; multiple comparisons; graphical methods for visualising data and checking (S)MA assumptions; robust (S)MA estimation and inference tools.
Multiple-group principal component analysis and discriminant analysis were used to investigate the morphological differences between adult skulls of male and female minks, badgers and otters from Norway. The first principal component axis, calculated from the variance-covariance matrix of log-transformed data, was interpreted as a growth-free size axis in all three species, while the other components were interpreted as representing shape. Having largely separated size and shape variation, these two aspects of sexual dimorphism could be studied. The standardized component scores were subjected to an analysis of variance and discriminant analyses were performed on size-in and size-out data. Sexual dimorphism was disclosed on eight of the 12 components in minks and on seven of the 12 components in badgers and otters. In mink the multivariate differences were more due to size than to shape, whereas in badgers and otters most of the multivariate differences were due to shape, but the differences in size were also significant. The shape dimorphism was shown to be functionally related to jaw and neck muscles. The results were discussed in relation to recent theories to explain the evolutionary significance of sexual dimorphism in body size of mustelids. It was concluded that these theories do not fully explain the dimorphism found in the skulls of the moderately dimorphic badger and otter.
Fifteen functionally significant aspects of skull morphology were measured on skulls of 36 additional species of carnivores to complete a survey of skull shape in modern fissiped (land) carnivores that includes most of the living genera. The measurements were transformed to dimensionless variables based on the residuals from allometric equations, and were analysed singly and in a 10 variable principal components analysis. An initial study of 62 species of viverrids, canids, mustelids and felids had shown those families to be distinguished from each other by the functionally significant measurements. However, among the additional 36 species, some procyonids, ursids and mustelids display a range of diversity of skull morphology that overlaps that of the other families and diminishes the potential value of the measurements as taxonomic characters. Intraspecific variation is presented for 12 species, and is low enough to allow use of some features as species level diagnostic characters. The lack of correlation between diet and functionally significant aspects of skull morphology among omnivorous carnivores, and the absence of certain skull shapes among carnivores are discussed.
Fifteen variables, selected primarily to reflect functionally significant aspects of cranial morphology, were measured on one skull each of 62 species of modern carnivores, including viverrids, canids, mustelids and felids. To allow comparisons between species of different sizes without the potentially confounding effects of allometric shape changes, the measurements were transformed to dimensionless variables, based on the residuals from allometric equations. Fourteen out of 15 of the transformed variables distinguish one or more of the four family groups and the rotated first two axes of a principal components analysis distinguish all four families from each other. The following functional hypotheses are proposed: mustelids and felids have the most powerful bites and canids the weakest among the four family groups studied; mustelids and, to a lesser degree, felids have more powerful neck musculature than do canids and viverrids; and visual abilities are best developed among felids and least developed among mustelids. The first two functional hypotheses suggest possible differences in killing behaviour, which are supported by a preliminary survey of the literature on such behaviour. Allometric analysis of the 15 cranial measures shows that the neurocranial components scale with negative allometry, while most of the other measures scale approximately isometrically.
Nearly all animals show altered musculo-skeletal phenotypes when subjected to captive conditions. Whether such changes affect biomechanical performance is for the most part unknown. In American alligators Alligator mississippiensis such modifications include shortened jaws, more robust body form, and broadened heads. Bite-force performance was assessed for a variety of sizes of wild-captured alligator specimens and the results correlated with morphological indices. Bite forces ranged from 217 to 13 172 N, with the latter being the highest value ever measured for a living animal. These data were statistically compared with those for long-term captive specimens using ANCOVA. Bite-force performance showed similar patterns of increase between captive and wild-reared animals, and bite forces with respect to snout–vent length and body mass were statistically indistinguishable. Nevertheless, with respect to head size, captive alligators were found to bite more forcefully than their wild counterparts. These findings illustrate the importance of considering biomechanical performance differences between wild and captive individuals if meaningful ecological ties are to be made. Furthermore, before concluding that wild-reared or captive animals show similar or different biomechanical performances, it is important to understand that standardization to different morphological parameters can reveal conflicting results. Consideration as to which measures are the most germane to the question at hand is essential.
Summary 1. Morphological characteristics (snout-vent length, badge area, mass, limb and head measures) and whole-animal performance capacities (sprint speed, acceleration capacity, stamina and bite force) were measured in male lizards, Gallotia galloti . These males were also tested in paired staged contests to assess relative fighting capacity and to link these results to morphology and performance. 2. A multivariate analysis of the four performance features revealed a clear difference between the physiological capacities of winners vs losers, with bite force being the most important predictor of the outcome of fights. 3. The finding that bite performance is linked to dominance fits in with the high sexual dimorphism in head size in this species, as head size is a predictor of bite force performance. 4. Winners of contests also tended to have larger total areas of blue patches on their sides, suggesting that these badges convey information on the social status of the males. However, since no correlation was found between bite force and badge size, the patches seem to contain information on a component of fighting capacity other than bite force.
Skull variables were analysed for allometry patterns in 56 species of extant carnivores. As previously reported, many skull variables scale near isometrically with either skull length or lower jaw length. The maximal gape angle scales insignificantly (P<0.05) with skull size, but the clearance between the canines shows a significant relationship with skull size and scales near isometrically. Maximal bite forces were estimated from geometrical cross-sectional areas of dried skulls, and the bending strength of the canines was computed by modelling the canines as a cantilevered beam of solid, homogeneous material with an elliptical cross section. Previous hypotheses of large taxon differences in canine bending strengths, so that felids have stronger canines than canids, are corroborated when actual bite forces at the upper canine are ignored. Incorporation of bite force values, however, nullifies the differences in canine bending strength among felids and canids, and ursids seem to have stronger canines than felids. This is probably because of the significantly longer canines of felids compared to canids and ursids, and the generally high bite forces of felids.
1. In vertebrates, bite force is a measure of whole organism performance that is associated with both cranial morphology and dietary ecology. Mechanistic studies of bite force production have identified morphological features associated with bite force, and linked bite force with diet, but this approach has rarely been used in mammals.
2. Mammals are a good system with which to investigate the function of the feeding apparatus because of the relative simplicity of their skulls and their high dietary diversity. Phyllostomid bats are one of the most trophically and morphologically diverse groups of mammals, but we know little about the relative importance of biomechanical variables in producing bite force or how these variables vary with diet.
3. We combined in vivo measurements of bite force with assessments of muscular and bony morphology to build and validate a model describing the mechanics of bite force production in 25 species of bats. We used this model to investigate how bats with different diets vary in biomechanical parameters that contribute to bite force. In addition to traditional dietary categories, we used a functional definition of diet that reflects the mechanical demands (hardness) of the food items in the natural diet.
4. Our model provided good predictions of in vivo bite forces and highlighted behavioural variation that is inherent in the in vivo data. The temporalis generates the highest moment about the temporomandibular joint (TMJ) axis, but the moment generated by the masseter is the most important variable in explaining variation among species. The dietary classification based on the hardness of the diet was more effective than traditional dietary categories in describing biomechanical differences among groups. The temporalis generated the highest proportion of the moment about the TMJ axis in species with very hard and hard diets, the masseter was most important for species with soft diets, and the medial pterygoid was most important for species with liquid diets.
5. Our results highlight the utility of combining a modelling approach with in vivo data when conducting ecomorphological studies, and the importance of ecological classifications that reflect functional importance of performance traits.
We illustrate here microCT images in which contrast between muscle and connective tissue has been achieved by means of staining with iodine. Enhancement is shown to be dependent on the concentration of iodine solution (I(2)KI), time in solution and specimen size. Histological examination confirms that the arrangement of individual muscle fibres can be visualised on the enhanced microCT images, and that the iodine accumulates in the muscle fibres in preference to the surrounding connective tissues. We explore the application of this technique to describe the fibrous structure of skeletal muscle, and conclude that it has the potential to become a non-destructive and cost-effective method for investigating muscle fascicle architecture, particularly in comparative morphological studies.
A key question in evolution is the degree to which morphofunctional complexes are constrained by phylogeny. We investigated the role of phylogeny in the evolution of biting performance, quantified as bite forces, using phylogenetic eigenvector regression. Results indicate that there are strong phylogenetic signals in both absolute and size-adjusted bite forces, although it is weaker in the latter. This indicates that elimination of size influences reduces the level of phylogenetic inertia and that the majority of the phylogenetic constraint is a result of size. Tracing the evolution of bite force through phylogeny by character optimization also supports this notion, in that relative bite force is randomly distributed across phylogeny whereas absolute bite force diverges according to clade. The nonphylogenetically structured variance in bite force could not be sufficiently explained by species-unique morphology or by ecology. This study demonstrates the difficulties in identifying causes of nonphylogenetically structured variance in morphofunctional character complexes.
Thesis (Ph. D. in anatomy)--University of Illinois at the Medical Center, 1968.
The purpose of this paper is to analyse the effects of cranial size and shape in domestic dogs (Canis familiaris) on predicted forces of biting. In addition to continuous size-shape analysis, nine size-shape groups were developed based on three skull shape categories and three skull size categories. Bite forces were predicted from measurements made on dried skulls using two lever models of the skull, as well as simple models derived by regression analysis. Observed bite force values were not available for the database used in this study, so only comparisons between categories and models were undertaken. The effects of shape and size on scaled predicted bite forces were evaluated. Results show that bite force increases as size increases, and this effect was highly significant (P < 0.0001). The effect of skull shape on bite force was significant in medium and large dogs (P < 0.05). Significant differences were not evident in small dogs. Size x shape interactions were also significant (P < 0.05). Bite force predictions by the two lever models were relatively close to each other, whereas the regression models diverged slightly with some negative numbers for very small dogs. The lever models may thus be more robust across a wider range of skull size-shapes. Results obtained here would be useful to the pet food industry for food product development, as well as to paleontologists interested in methods of estimating bite force from dry skulls.