Musculoskeletal anatomy of the Eurasian lynx,Lynx lynx (Carnivora: Felidae) forelimb: Adaptations to capture large prey?

Mammalian carnivores adhere to two different feeding strategies relative to their body masses. Large carnivores prey on animals that are the same size or larger than themselves, whereas small carnivores prey on smaller vertebrates and invertebrates. The Eurasian lynx (Lynx lynx) falls in between these two categories. Lynx descend from larger forms that were probably large prey specialists, but during the Pleistocene became predators of small prey. The modern Eurasian lynx may be an evolutionary reversal toward specializing in large prey again. We hypothesized that the musculoskeletal anatomy of lynx should show traits for catching large prey. To test our hypothesis, we dissected the forelimb muscles of six Eurasian lynx individuals and compared our findings to results published for other felids. We measured the bones and compared their dimensions to the published material. Our material displayed a well‐developed pectoral girdle musculature with some uniquely extensive muscle attachments. The upper arm musculature resembled that of the pantherine felids and probably the extinct sabertooths, and also the muscles responsible for supination and pronation were similar to those in large cats. The muscles controlling the pollex were well‐developed. However, skeletal indices were similar to those of small prey predators. Our findings show that lynx possess the topographic pattern of muscle origin and insertion like in large felids. J. Morphol. 277:753–765, 2016. © 2016 Wiley Periodicals, Inc.     

Feeding ecology and morphology of the upper canines in bears (carnivora: Ursidae)

The morphology and mechanical strength of the upper canines in all eight extant species of ursids is analyzed, and the findings are discussed in relation to feeding ecology. Ursids have proportionally smaller canines than other large carnivores with a specialized feeding ecology, such as large felids, and the upper canine morphology is both canid‐like and felid‐like. The giant panda is the most divergent species, and its short, blunt, and cone‐like canines appear well adapted for tearing into bamboo. The almost equally herbivorous spectacled bear has a less derived canine morphology. The large canines of the sun bear are divergent from other ursine ursids, and may be an adaptation for tearing open tree trunks in search of insects. Discriminant Analysis is successful in separating ursid species on the basis of canine morphology, but the canines of ursine ursids, and also of the spectacled bear, show greater resemblance among the species than the marked differences in feeding ecology would suggest. This could be in part due to a short evolutionary history, and in part due to canines not having been subjected to much evolutionary selection as has been the case among other large carnivores, such as large felids. Ursids are probably evolutionarily and ecologically successful due to physical size and strength rather than a derived craniodental anatomy. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

EMG of the digastric muscle in gibbon and orangutan: Functional consequences of the loss of the anterior digastric in orangutans

Unlike all other primates, the digastric muscle of the orangutan lacks an anterior belly; the posterior belly, while present, inserts directly onto the mandible. To understand the functional consequences of this morphologic novelty, the EMG activity patterns of the digastric muscle and other potential mandibular depressors were studied in a gibbon and an orangutan. The results suggest a significant degree of functional differentiation between the two digastric bellies. In the gibbon, the recruitment pattern of the posterior digastric during mastication is typically biphasic. It is an important mandibular depressor, active in this role during mastication and wide opening. It also acts with the anterior suprahyoid muscles to move the hyoid prior to jaw opening during mastication. The recruitment patterns of the anterior digastric suggest that it is functionally allied to the geniohyoid and mylohyoid. For example, although it transmits the force of the posterior digastric during mandibular depression, it functions independent of the posterior digastric during swallowing. Of the muscles studied, the posterior digastric was the only muscle to exhibit major differences in recruitment pattern between the two species. The posterior digastric retains its function as a mandibular depressor in orangutans, but is never recruited biphasically, and is not active prior to opening. The unique anatomy of the digastric muscle in orangutans results in decoupling of the mechanisms for hyoid movement and mandibular depression, and during unilateral activity it potentially contributes to substantial transverse movements of the mandible. Hypotheses to explain the loss of the anterior digastric should incorporate these functional conclusions. © 1994 Wiley-Liss, Inc.     

Mechanics of biting in great white and sandtiger sharks

Although a strong correlation between jaw mechanics and prey selection has been demonstrated in bony fishes (Osteichthyes), how jaw mechanics influence feeding performance in cartilaginous fishes (Chondrichthyes) remains unknown. Hence, tooth shape has been regarded as a primary predictor of feeding behavior in sharks. Here we apply Finite Element Analysis (FEA) to examine form and function in the jaws of two threatened shark species, the great white (Carcharodon carcharias) and the sandtiger (Carcharias taurus). These species possess characteristic tooth shapes believed to reflect dietary preferences. We show that the jaws of sandtigers and great whites are adapted for rapid closure and generation of maximum bite force, respectively, and that these functional differences are consistent with diet and dentition. Our results suggest that in both taxa, insertion of jaw adductor muscles on a central tendon functions to straighten and sustain muscle fibers to nearly orthogonal insertion angles as the mouth opens. We argue that this jaw muscle arrangement allows high bite forces to be maintained across a wider range of gape angles than observed in mammalian models. Finally, our data suggest that the jaws of sub-adult great whites are mechanically vulnerable when handling large prey. In addition to ontogenetic changes in dentition, further mineralization of the jaws may be required to effectively feed on marine mammals. Our study is the first comparative FEA of the jaws for any fish species. Results highlight the potential of FEA for testing previously intractable questions regarding feeding mechanisms in sharks and other vertebrates.     

The functional significance of primate mandibular form.

A stress analysis of the primate mandible suggests that vertically deep jaws in the molar region are usually an adaptation to counter increased sagittal bending stress about the balancing-side mandibular corpus during unilateral mastication. This increased bending stress about the balancing side is caused by an increase in the amount of balancing-side muscle force. Furthermore, this increased muscle force will also cause an increase in dorso-ventral shear stress along the mandibular symphysis. Since increased symphyseal stress can be countered by symphyseal fusion and as increased bending stress can be countered by a deeper jaw, deep jaws and symphyseal fusion are often part of the same functional pattern. In some primates (e.g., Cercocebus albigena), deep jaws are an adaptation to counter bending in the sagittal plane during powerful incisor biting, rather than during unilateral mastication. The stress analysis of the primate mandible also suggests that jaws which are transversely thick in the molar region are an adaptation to counter increased torsion about the long axis of the working-side mandibular corpus during unilateral mastication. Increased torsion of the mandibular corpus can be caused by an increase in masticatory muscle force, an increase in the transverse component of the postcanine bite force and/or an increase in premolar use during mastication. Patterns of masticatory muscle force were estimated for galagos and macaques, demonstrating that the ratio of working-side muscle force to balancing-side muscle force is approximately 1.5:1 in macaques and 3.5:1 in galagos during unilateral isometric molar biting. These data support the hypothesis that mandibular symphyseal fusion is an adaptative response to maximize unilateral molar bite force by utilizing a greater percentage of balancing-side muscle force.     

Previously undescribed features in the temporalis and masseteric musculature of several large felids raised in captivity

Although the anatomy of the domestic housecat has been examined in meticulous detail, comparative observations on the anatomy of the larger wild cats is scant and information about particularities in their cranial complexes rarer still. In the course of dissecting sets of masticatory muscles in five large felids, all older zoo animals, we had the opportunity to note muscular attachments in the head and jaw apparatus that appeared significantly broader and more distal in their insertion sties than expected. Further investigation may determine whether these masticatory peculiarities are functional adaptations of felids, or instead are associated in some manner with the specialized diets large felids receive in captive environments. Zoo Biol 16:187–191, 1997. © 1997 Wiley-Liss, Inc.     

Neuromechanisms of reciprocal interrelation between jaw-opening and jaw-closing muscles in the cat (author's transl)]

Neural controlling mechanisms between the digastric (jaw-opening) and masseter (jaw-closing) muscles were studied in the cat. High threshold afferent impulses from the anterior belly of the digastric muscle to masseteric montoneurons in the trigeminal motor nucleus induced an EPSP-IPSP sequence of potentials with long latency, and high threshold afferent impulses from the masseter muscle also exerted a similar effect on digastric motoneurons in the same nucleus innervating the anterior belly of the digastric muscle. These results suggest that reciprocal inhibition via Ia interneurons as observed between the flexor and extensor muscles in the spinal cord does not exist between the digastric and masseter muscles in the cat. However, the respective motoneurons innervating the masseter and digastric muscles receive inputs of early excitation-late inhibition via high threshold afferent nerve fibers from each antagonistic muscle. As such, since EPSPs preceding IPSPs are recognized, these high threshold afferent impulses may exert not only a reciprocal inhibitory effect, but also a synchronous excitatory or inhibitory effect on the antagonistic motoneurons.     

Evolution of skull shape in carnivores 1. Representative modern carnivores

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.     

A dynamic model for the evolution of sabrecat predatory bite mechanics

The ability of sabretoothed felids to achieve sufficiently high bite forces for predation at extreme gape angles has been the subject of decades of debate. Previous studies have indicated that bite forces in derived sabretoothed felids would have been low, but that they were probably augmented by head depressing muscles. However, bite mechanics is a dynamic process, and mechanical properties change with changes in gape angles. In this study, I present the first comprehensive model of bite mechanics, vector angles, and forces about the temporomandibular joint at gape angles from occlusion to maximal inferred gape in sabretoothed felids. Primitive sabrecats (Machairodus, Paramachairodus) appear broadly comparable to extant large felids (Panthera, Puma), but derived sabrecats in the groups Homotherini (Amphimachairodus, Homotherium, Xenosmilus) and Smilodontini (Megantereon, Smilodon) are often substantially different from either of the former. The ability of the mandibular adductors to generate torque changes with gape angle, indicating that previous models fail to capture potentially important differences in bite function. Inferred muscle sizes and the angles of effective torque from individual adductor fibres in derived sabrecats are different from those of primitive sabrecats and extant large felids, but they had evolved a number of compensatory adaptations for maximizing force output at the canine and carnassial, primarily changes in muscle fibre angles and more compact crania. Inferred outforces at the canines and carnassials were comparable amongst all groups at low gape angles, but at extreme gape angles outforces would have been low, supporting previous hypotheses of head flexor contribution during initial stages of the killing bite in sabrecats. Mandibular adduction in extant carnivores is a complicated pattern of differences in twitch tension and electromyographical activity at different gape angles, and inference of maximal isotonic bite forces from reconstructed mandibular adductor sizes in fossils will give estimates primarily suitable for comparative purposes. Potentially, derived sabrecats could have evolved differences from extant felids in adductor histochemistry or pinnation angle of individual fibres. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 220–242.     

Comparative myology of the hominoid cranial base. I. The muscular relationships and bony attachments of the digastric muscle

This paper aims to document accurately the soft tissue anatomy and bony attachments of the posterior belly of the digastric muscle and other closely related muscles in the mastoid region of extant hominoids and fossil hominids. Five wet specimens including individuals of Pan, Gorilla and Pongo were dissected and described. Eight casts of fossil hominid cranial bases were also studied along with measurements and notes made from the same original fossil hominid specimens to assess their soft tissue markings in the light of the findings for the three great apes. The results indicate that whereas the attachment of the posterior belly of the digastric muscle in Homo sapiens is associated with a deep groove or fossa, it originates from a widened area and leaves no bony markings on the cranial base of the three great apes. Following a change in the position of the foramen magnum and the occipital condyles in hominids and H. sapiens the insertion of the posterior belly of the digastric has remained posteriorly positioned but has become compressed into a deep groove. It is likely that this has come about by the displacement of the more medial soft tissue structures which have been moved laterally away from the occipital condyles.     

Functional morphology of the pharyngeal jaw apparatus in perciform fishes: An experimental analysis of the haemulidae

A new mechanical model for function of the pharyngeal jaw apparatus in generalized perciform fishes is developed from work with the family Haemulidae. The model is based on anatomical observations, patterns of muscle activity during feeding (electromyography), and the actions of directly stimulated muscles. The primary working stroke of the pharyngeal apparatus involves simultaneous upper jaw depression and retraction against a stabilized and elevating lower jaw. The working stroke is characterized by overlapping activity in most branchial muscles and is resolved into three phases. Four muscles (obliquus dorsalis 3, levator posterior, levator externus 3/4, and obliquus posterior) that act to depress the upper jaws become active in the first phase. Next, the retractor dorsalis, the only upper jaw retracting muscle, becomes active. Finally, there is activity in several muscles (transversus ventrales, pharyngocleithralis externus, pharyngohyoideus, and protractor pectoralis) that attach to the lower jaws. The combined effect of these muscles is to elevate and stabilize the lower jaws against the depressing and retracting upper jaws. The model identifies a novel mechanism of upper jaw depression, here proposed to be the primary component of the perciform pharyngeal jaw bite. The key to this mechanism is the joint between the epibranchial and toothed pharyngobranchial of arches 3 and 4. Dorsal rotation of epibranchials 3 and 4 about the insertion of the obliquus posterior depresses the lateral border of pharyngobranchials 3 and 4 (upper jaw). The obliquus dorsalis 3 muscle crosses the epibranchial-pharyngo-branchial joint in arches 3 and 4, and several additional muscles effect epibranchial rotation. Five upper jaw muscles cause upper jaw depression upon electrical stimulation: the obliquus dorsalis 3, levator posterior, levator externus 3/4, obliquus posterior, and transversus dorsalis. This result directly contradicts previous interpretations of function for the first three muscles. The presence of strong depression of the upper pharyngeal jaws explains the ability of many generalized perciform fishes to crush hard prey in their pharyngeal apparatus.     

Sarcocysts in the Florida bobcat (Felis rufus floridanus).

Sarcocysts were found in the tongue, diaphragm, heart, intestinal tunica muscularis, and skeletal muscle of bobcats (Felis rufus floridanus) collected in Florida (USA). The tongue was found to be the best indicator tissue for sarcocysts (P less than 0.005). Thirty of 60 bobcats screened were found to contain sarcocysts in at least one of the muscle tissues examined. Of the positive bobcats, 28 of 28 tongues contained sarcocysts, while only 10 of 27 (37%), and 8 of 26 (31%) contained sarcocysts in the diaphragm or cardiac muscle, respectively. Although immune suppression has been suggested as a possible reason for formation of sarcocysts in some carnivores, no such correlation was evident in the bobcats. Comparisons of prey species taken by the panther and bobcat, and overlap of geographical range by the two species leave questions as to the source of infection, and the species of Sarcocystis that is infecting both felids.     

Implications of the mastoid anatomy of larger extant felids for the evolution and predatory behaviour of sabretoothed cats (Mammalia, Carnivora, Felidae)

Muscle attachments in the mastoid region of the skull of extant felids are studied through dissection of two adult tigers Panthera tigris (Linnaeus, 1758) Pocock, 1930, a lion Panthera leo (Linnaeus, 1758) Pocock, 1930 and a puma Puma concolor (Linnaeus, 1771) Jardine, 1834, providing for the first time an adequate reference for the study of the evolution of that region in sabretoothed felids. Our study supports the inference by W. Akersten that the main muscles inserting in the mastoid process in sabretooths were those originating in the atlas, rather than those from the posterior neck, sternum and forelimb. Those inferences were based on the anatomy of the giant panda, Ailuropoda melanoleuca (David, 1869) Milne-Edwards, 1870, raising uncertainties about homology, which were founded, as revealed by our results. The mastoid muscle insertions in extant felids differ in important details from those described for Ailuropoda , but agree with those described for domestic cats, hyenas and dogs. The large, antero-ventrally projected mastoid process of pantherines allows a moderate implication of the m. obliquus capitis anterior in head-flexion. This contradicts the widespread notion that the function of this muscle in carnivores is to extend the atlanto-cranial joint and to flex it laterally, but supports previous inferences about the head-flexing function of atlanto-mastoid muscles in machairodontines. Sabretooth mastoid morphology implies larger and longer-fibred atlanto-mastoid muscles than in pantherines, and that most of their fibres ran inferior to the axis of rotation of the atlanto-occipital joint, emphasizing head-flexing action.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 140 , 207–221.     

Anatomical anomaly of human digastric muscles

In the submandibular region an anatomical anomaly of muscle arrangement was found. Between the left and right digastric muscles, asymmetric accessory digastric muscles were detected, which all arose from the mandible and were attached to the hyoid bone. Furthermore, the right anterior digastric muscle had an accessory belly. These anomalies of digastric muscles may be anatomical manifestations of a functional support of the mylohyoid muscle.     

Correlation of carnassial tooth size and body weight in recent carnivores (mammalia)

The correlation between the lower carnassial crown area and the body weight is examined for modern carnivores. It is very high, but the ursids and felids show a relationship different from the other carnivore families. Some exceptions are discussed. The possibility of predicting body weight for fossils is given.     

The structure of the mandibular corpus and its relationship to feeding behaviours in extant carnivorans

Assuming some optimization of bone structure to applied mechanical loadings in vivo , different killing and feeding behaviours in carnivores should be reflected in observed differences in cross-sectional shape of their mandibular corpora. Section moduli are used to gauge the magnitudes of bending moments in the mandibular corpus and, when dentary length is controlled, the magnitudes of forces applied to the corpus. Comparisons are made of section moduli at the P₃P₄ and P₄M₁ interdental gaps among canids, felids and hyaenids; in canids only, the M₁M₂ interdental gap was also studied. Local variations in loadings are identified by comparing the section moduli at adjacent loci along the corpus within each family.
The findings of this study show that the precarnassial corpora of canids and hyaenids have greater strength in bending than the corpora of felids of similar body weight. This is taken to reflect relatively greater bending moments under loading in the corpora of canids and hyaenids due, in part, to their elongate dentaries (relative to body weight). Relative to dentary length , however, the precarnassial corpora of felids and hyaenids have much greater strength in bending than the corpora of canids. These scaling relationships appear to reflect the high customary forces (i.e. not moments) applied to the precarnassial corpora of felids and hyaenids with sustained canine killing bites and with bone ingestion using the premolars, respectively. An increase in bending strength of the corpus caudal to the camassial blade in canids is interpreted to be an adaptation for bone-crushing with the postcarnassial molars.     

Evolution of skull shape in carnivores 2. Additional modern carnivores

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.     

Feeding biomechanics in Acanthostega and across the fish–tetrapod transition

Acanthostega is one of the earliest and most primitive limbed vertebrates. Its numerous fish-like features indicate a primarily aquatic lifestyle, yet cranial suture morphology suggests that its skull is more similar to those of terrestrial taxa. Here, we apply geometric morphometrics and two-dimensional finite-element analysis to the lower jaws of Acanthostega and 22 other tetrapodomorph taxa in order to quantify morphological and functional changes across the fish–tetrapod transition. The jaw of Acanthostega is similar to that of certain tetrapodomorph fish and transitional Devonian taxa both morphologically (as indicated by its proximity to those taxa in morphospace) and functionally (as indicated by the distribution of stress values and relative magnitude of bite force). Our results suggest a slow tempo of morphological and biomechanical changes in the transition from Devonian tetrapod jaws to aquatic/semi-aquatic Carboniferous tetrapod jaws. We conclude that Acanthostega retained a primitively aquatic lifestyle and did not possess cranial adaptations for terrestrial feeding.     

Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil

Natural hybrid zones between distinct species have been reported for many taxa, but so far, few examples involve carnivores or Neotropical mammals in general. In this study, we employed mitochondrial DNA (mtDNA) sequences and nine microsatellite loci to identify and characterize a hybrid zone between two Neotropical felids, Leopardus geoffroyi and L. tigrinus, both of which are well-established species having diverged from each other c. 1 million years ago. These two felids are mostly allopatric throughout their ranges in South America, with a narrow contact zone that includes southern Brazil. We present strong evidence for the occurrence of hybridization between these species and identify at least 14 individuals (most of them originating from the geographical contact zone) exhibiting signs of interspecific genomic introgression. The genetic structure of Brazilian L. tigrinus populations seems to be affected by this introgression process, showing a gradient of differentiation from L. geoffroyi correlated with distance from the contact zone. We also corroborate and extend previous findings of hybridization between L. tigrinus and a third related felid, L. colocolo, leading to an unusual situation for a mammal, in which the former species contains introgressed mtDNA lineages from two distinct taxa in addition to its own.     

Trophic Cascades in Terrestrial Systems: A Review of the Effects of Carnivore Removals on Plants

We present a quantitative synthesis of trophic cascades in terrestrial systems using data from 41 studies, reporting 60 independent tests. The studies covered a wide range of taxa in various terrestrial systems with varying degrees of species diversity. We quantified the average magnitude of direct effects of carnivores on herbivore prey and indirect effects of carnivores on plants. We examined how the effect magnitudes varied with type of carnivores in the study system, food web diversity, and experimental protocol. A metaanalysis of the data revealed that trophic cascades were common among the studies. Exceptions to this general trend did arise. In some cases, trophic cascades were expected not to occur, and they did not. In other cases, the direct effects of carnivores on herbivores were stronger than the indirect effects of carnivores on plants, indicating that top-down effects attenuated. Top-down effects usually attenuated whenever plants contained antiherbivore defenses or when herbivore species diversity was high. Conclusions about the strength of top-down effects of carnivores varied with the type of carnivore and with the plant-response variable measured. Vertebrate carnivores generally had stronger effects than invertebrate carnivores. Carnivores, in general, had stronger effects when the response was measured as plant damage rather than as plant biomass or plant reproductive output. We caution, therefore, that conclusions about the strength of top-down effects could be an artifact of the plant-response variable measured. We also found that mesocosm experiments generally had weaker effect magnitudes than open-plot field experiments or observational experiments. Trophic cascades in terrestrial systems, although not a universal phenomenon, are a consistent response throughout the published studies reviewed here. Our analysis thus suggests that they occur more frequently in terrestrial systems than currently believed. Moreover, the mechanisms and strengths of top-down effects of carnivores are equivalent to those found in other types of systems (e.g., aquatic environments).