Andrew J. Clark

Morphology and kinematics of feeding in hagfish: possible functional advantages of jaws

SUMMARY As in gnathostomes, the hagfish feeding apparatus includes skeletal, dental and muscular components. In the present study, we examined feeding morphology and kinematics in two hagfish species, Eptatretus stoutii and Myxine glutinosa, representing the two major hagfish lineages. E. stoutii have larger dental plates, larger basal plates, and stronger clavatus muscles (the major dental plate retractor) than M. glutinosa. Despite morphological differences, kinematic profiles are similar in E. stoutii and M. glutinosa. When protracted, the dental plate unfolds and exposes keratinous teeth, which are then embedded in the prey. Once food is grasped, the dental plate is retracted into the mouth. During retraction, the clavatus muscle can generate up to 16 N of force, which exceeds the bite force of some gnathostomes of similar size. In addition to producing high forces with the feeding muscles, hagfish can evert their dental plates to 180°, exceeding the gape angles attained by virtually all gnathostomes, suggesting vertebrate jaws are not the prerequisites for muscle force generation and wide gapes. We propose that dental plate protraction and retraction can be modeled as a fixed pulley that lacks the speed amplification occurring in gnathostome jaws. Hagfish gape cycle times are approximately 1 s, and are longer than those of gnathostomes, suggesting that a functional advantage of jaws is the speed that allows gnathostomes to exploit elusive prey.

Slipping, sliding and stability: locomotor strategies for overcoming low-friction surfaces.

SUMMARY Legged terrestrial animals must avoid falling while negotiating unexpected perturbations inherent to their structurally complex environments. Among humans, fatal and nonfatal injuries frequently result from slip-induced falls precipitated by sudden unexpected encounters with low-friction surfaces. Although studies using walking human models have identified some causes of falls and mechanisms underlying slip prevention, it is unclear whether these apply to various locomotor speeds and other species. We used high-speed video and inverse dynamics to investigate the locomotor biomechanics of helmeted guinea fowl traversing slippery surfaces at variable running speeds (1.3–3.6 m s–1). Falls were circumvented when limb contact angles exceeded 70 deg, though lower angles were tolerated at faster running speeds (>3.0 m s–1). These prerequisites permitted a forward shift of the bodys center of mass over the limbs base of support, which kept slip distances below 10 cm (the threshold distance for falls) and maximized the vertical ground reaction forces, thus facilitating limb retraction and the conclusion of the stance phase. These postural control strategies for slip avoidance parallel those in humans, demonstrating the applicability of these strategies across locomotor gaits and the potential for guinea fowl as an insightful model for invasive approaches to understanding limb neuromuscular control on slippery surfaces.

Ontogenetic scaling of the morphology and biomechanics of the feeding apparatus in the Pacific hagfish Eptatretus stoutii

The form and function of the support skeleton, musculature and teeth were examined in an ontogenetic series of Pacific hagfish Eptatretus stoutii spanning about a six-fold range in total length (L(T)). Tooth area, feeding apparatus length, basal plate size, theoretical dental plate retractile force, penetration force and applied tooth stress were measured relative to body size. Morphological variables (e.g. tooth area and basal plate size) scaled with positive allometry and functional variables (e.g. retractile force and applied tooth stress) scaled isometrically with L(T). These results suggest that juveniles do not undergo ontogenetic dietary changes and consume functionally equivalent prey to adults, although adults can grasp proportionally larger portions of food. Low tooth stress in juveniles and adults imposes mechanical constraints to puncturing and tearing, which are circumvented by a preference for softer prey tissue or the inclusion of knotting behaviours for reducing tougher prey.

Mechanical properties of the cuticles of three cockroach species that differ in their wind-evoked escape behavior

The structural and material properties of insect cuticle remain largely unexplored, even though they comprise the majority (approximately 80%) of animals. Insect cuticle serves many functions, including protection against predatory attacks, which is especially beneficial to species failing to employ effective running escape responses. Despite recent advances in our understanding of insect escape behaviors and the biomechanics of insect cuticle, there are limited studies on the protective qualities of cuticle to extreme mechanical stresses and strains imposed by predatory attacks, and how these qualities vary between species employing different escape responses. Blattarians (cockroaches) provide an appropriate model system for such studies. Wind-evoked running escape responses are strong in Periplaneta americana, weak in Blaberus craniifer and absent in Gromphodorhina portentosa, putting the latter two species at greater risk of being struck by a predator. We hypothesized that the exoskeletons in these two larger species could provide more protection from predatory strikes relative to the exoskeleton of P. americana. We quantified the protective qualities of the exoskeletons by measuring the puncture resistance, tensile strength, strain energy storage, and peak strain in fresh samples of thoracic and abdominal cuticles from these three species. We found a continuum in puncture resistance, tensile strength, and strain energy storage between the three species, which were greatest in G. portentosa, moderate in B. craniifer, and smallest in P. americana. Histological measurements of total cuticle thickness followed this same pattern. However, peak strain followed a different trend between species. The comparisons in the material properties drawn between the cuticles of G. portentosa, B. craniifer, and P. americana demonstrate parallels between cuticular biomechanics and predator running escape responses.

A soft origin for a forceful bite: motor patterns of the feeding musculature in Atlantic hagfish, Myxine glutinosa

Despite lacking jaws and substantial rigid support for feeding muscles, hagfishes can forcefully grasp and ingest chunks of flesh from their prey. When feeding, bilaterally folding dental plates protrude from the mouth, then forcefully retract. This cyclic protraction and retraction occurs in the anterior region of the hagfish feeding apparatus (HFA) and involves both a cartilaginous skeleton and a complex array of muscles that act as a hydrostat. We recorded motor patterns from the largest muscles in the HFA in six specimens of Myxine glutinosa: the deep protractor muscle (DPM), clavatus muscle (CM), perpendicularis muscle (PM), and tubulatus muscle (TM). Individuals normally used four gape cycles to ingest food and four gape cycles to intraorally transport food. We measured burst duration from each muscle and the onsets of kinematic events and the onsets of CM, PM, and TM bursts relative to the onset of the DPM. The DPM fired during protraction, while the CM, PM and TM fired during retraction. Our study corroborates our anatomical predictions about DPM and CM function. Activation of the circumferentially and vertically oriented fibers of the TM and PM stiffens the origin of the CM, allowing it to forcefully retract the dental plates. The progressive decrease in retractor muscle activity during gape cycles following ingestion suggests a reliance on passive properties of the musculoskeletal system for retraction.

Material Properties of Hagfish Skin, with Insights into Knotting Behaviors

Hagfishes (Myxinidae) often integrate whole-body knotting movements with jawless biting motions when reducing large marine carcasses to ingestible items. Adaptations for these behaviors include complex arrangements of axial muscles and flexible, elongate bodies without vertebrae. Between the axial muscles and the hagfish skin is a large, blood-filled subcutaneous sinus devoid of the intricate, myoseptal tendon networks characteristic of the taut skins of other fishes. We propose that the loose-fitting skin of the hagfish facilitates the formation and manipulation of body knots, even if it is of little functional significance to steady swimming. Hagfish skin is a relatively thick, anisotropic, multilayered composite material comprising a superficial, thin, and slimy epidermis, a middle dermal layer densely packed with fibrous tissues, and a deep subdermal layer comprised of adipose tissue. Hagfish skin is stiffer when pulled longitudinally than circumferentially. Stress-strain data from uniaxial tensile tests show that hagfish skins are comparable in tensile strength and stiffness to the taut skins of elongate fishes that do not engage in knotting behaviors (e.g., sea lamprey and penpoint gunnel). Sheath-core-constructed ropes, which serve as more accurate models for hagfish bodies, demonstrate that loose skin (extra sheathing) enhances flexibility of the body (rope). Along with a loose-fitting skin, the morphologies of hagfish skin parallel those of moray eels, which are also known for generating and manipulating figure-eight-style body knots when struggling with prey.

Nonnative Gracilaria vermiculophylla tetrasporophytes are more difficult to debranch and are less nutritious than gametophytes

Theory predicts that the maintenance of haplodiplontic life cycles requires ecological differences between the haploid gametophytes and diploid sporophytes, yet evidence of such differences remain scarce. The haplodiplontic red seaweed Gracilaria vermiculophylla has invaded the temperate estuaries of the Northern Hemisphere, where it commonly modifies detrital and trophic pathways. In native populations, abundant hard substratum enables spore settlement, and gametophyte:tetrasporophyte ratios are ~40:60. In contrast, many non‐native populations persist in soft‐sediment habitats without abundant hard substratum, and can be 90%–100% tetrasporophytic. To test for ecologically relevant phenotypic differences, we measured thallus morphology, protein content, organic content, “debranching resistance” (i.e., tensile force required to remove a branch from its main axis node), and material properties between male gametophytes, female gametophytes, and tetrasporophytes from a single, nonnative site in Charleston Harbor, South Carolina, USA in 2015 and 2016. Thallus length and surface area to volume ratio differed between years, but were not significantly different between ploidies. Tetrasporophytes had lower protein content than gametophytes, suggesting the latter may be more attractive to consumers. More force was required to pull a branch from the main axis of tetrasporophytes relative to gametophytes. A difference in debranching resistance may help to maintain tetrasporophyte thallus durability relative to gametophytes, providing a potential advantage in free‐floating populations. These data may shed light on the invasion ecology of an important ecosystem engineer, and may advance our understanding of life cycle evolution and the maintenance of life cycle diversity.

No support for Heincke's law in hagfish (Myxinidae): lack of an association between body size and the depth of species occurrence

This study tests for interspecific evidence of Heinckes law among hagfishes and advances the field of research on body size and depth of occurrence in fishes by including a phylogenetic correction and by examining depth in four ways: maximum depth, minimum depth, mean depth of recorded specimens and the average of maximum and minimum depths of occurrence. Results yield no evidence for Heinckes law in hagfishes, no phylogenetic signal for the depth at which species occur, but moderate to weak phylogenetic signal for body size, suggesting that phylogeny may play a role in determining body size in this group.