Nicolai Konow

Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes

Of the 5000 fish species on coral reefs, corals dominate the diet of just 41 species. Most (61%) belong to a single family, the butterflyfishes (Chaetodontidae). We examine the evolutionary origins of chaetodontid corallivory using a new molecular phylogeny incorporating all 11 genera. A 1759‐bp sequence of nuclear (S7I1 and ETS2) and mitochondrial (cytochrome b) data yielded a fully resolved tree with strong support for all major nodes. A chronogram, constructed using Bayesian inference with multiple parametric priors, and recent ecological data reveal that corallivory has arisen at least five times over a period of 12 Ma, from 15.7 to 3 Ma. A move onto coral reefs in the Miocene foreshadowed rapid cladogenesis within Chaetodon and the origins of corallivory, coinciding with a global reorganization of coral reefs and the expansion of fast‐growing corals. This historical association underpins the sensitivity of specific butterflyfish clades to global coral decline.

Prey-capture in Pomacanthus semicirculatus (Teleostei, Pomacanthidae): functional implications of intramandibular joints in marine angelfishes.

SUMMARY We examined prey-capture morphology and kinematics in the angelfish, Pomacanthus semicirculatus (Cuvier 1931), to evaluate the magnitude and role of functional specialisation. The feeding apparatus of P. semicirculatus possess three biomechanical mechanisms of particular interest: (1) a novel intramandibular joint, permitting dentary rotation and protruded jaw closure; (2) an opercular linkage facilitating mandible depression; and (3) a suspensorial linkage with two novel points of flexion, permitting anterior rotation of the suspensorium and augmenting mandible protrusion. Prey-capture kinematics were quantified using motion analysis of high-speed video, yielding performance profiles illustrating timing of onset, duration and magnitude of movement in these three biomechanical systems, and other variables traditionally quantified in studies of teleostean ram–suction feeding activity. Mandible depression and suspensorial rotation both augmented mandible protrusion, and coincided during jaw protrusion, typically increasing head length by 30%. Jaw closure appeared to result from contraction of the adductor mandibulae segment A2, which rotated the dentary by approximately 30° relative to the articular. This resulted in jaw closure with the mandible fully depressed and the jaws at peak-protrusion. Feeding events were concluded by a high-velocity jaw retraction (20–50 ms), and completed in 450–750 ms. Feeding kinematics and morphology of Pomacanthus differed from other biting teleosts, and more closely resemble some long-jawed ram–suction feeders. The structural and functional modifications in the Pomacanthus feeding apparatus are matched to an unusual diet of structurally resilient and firmly attached benthic prey.

Muscle power attenuation by tendon during energy dissipation.

An important function of skeletal muscle is deceleration via active muscle fascicle lengthening, which dissipates movement energy. The mechanical interplay between muscle contraction and tendon elasticity is critical when muscles produce energy. However, the role of tendon elasticity during muscular energy dissipation remains unknown. We tested the hypothesis that tendon elasticity functions as a mechanical buffer, preventing high (and probably damaging) velocities and powers during active muscle fascicle lengthening. We directly measured lateral gastrocnemius muscle force and length in wild turkeys during controlled landings requiring rapid energy dissipation. Muscle-tendon unit (MTU) strain was measured via video kinematics, independent of muscle fascicle strain (measured via sonomicrometry). We found that rapid MTU lengthening immediately following impact involved little or no muscle fascicle lengthening. Therefore, joint flexion had to be accommodated by tendon stretch. After the early contact period, muscle fascicles lengthened and absorbed energy. This late lengthening occurred after most of the joint flexion, and was thus mainly driven by tendon recoil. Temporary tendon energy storage led to a significant reduction in muscle fascicle lengthening velocity and the rate of energy absorption. We conclude that tendons function as power attenuators that probably protect muscles against damage from rapid and forceful lengthening during energy dissipation.

How tendons buffer energy dissipation by muscle

To decelerate the body and limbs, muscles lengthen actively to dissipate energy. During rapid energy-dissipating events, tendons buffer the work done on muscle by storing elastic energy temporarily, then releasing this energy to do work on the muscle. This elastic mechanism may reduce the risk of muscle damage by reducing peak forces and lengthening rates of active muscle

The series elastic shock absorber: tendon elasticity modulates energy dissipation by muscle during burst deceleration

During downhill running, manoeuvring, negotiation of obstacles and landings from a jump, mechanical energy is dissipated via active lengthening of limb muscles. Tendon compliance provides a ‘shock-absorber’ mechanism that rapidly absorbs mechanical energy and releases it more slowly as the recoil of the tendon does work to stretch muscle fascicles. By lowering the rate of muscular energy dissipation, tendon compliance likely reduces the risk of muscle injury that can result from rapid and forceful muscle lengthening. Here, we examine how muscle–tendon mechanics are modulated in response to changes in demand for energy dissipation. We measured lateral gastrocnemius (LG) muscle activity, force and fascicle length, as well as leg joint kinematics and ground-reaction force, as turkeys performed drop-landings from three heights (0.5–1.5 m centre-of-mass elevation). Negative work by the LG muscle–tendon unit during landing increased with drop height, mainly owing to greater muscle recruitment and force as drop height increased. Although muscle strain did not increase with landing height, ankle flexion increased owing to increased tendon strain at higher muscle forces. Measurements of the length–tension relationship of the muscle indicated that the muscle reached peak force at shorter and likely safer operating lengths as drop height increased. Our results indicate that tendon compliance is important to the modulation of energy dissipation by active muscle with changes in demand and may provide a mechanism for rapid adjustment of function during deceleration tasks of unpredictable intensity.

Membrane muscle function in the compliant wings of bats

Unlike flapping birds and insects, bats possess membrane wings that are more similar to many gliding mammals. The vast majority of the wing is composed of a thin compliant skin membrane stretched between the limbs, hand, and body. Membrane wings are of particular interest because they may offer many advantages to micro air vehicles. One critical feature of membrane wings is that they camber passively in response to aerodynamic load, potentially allowing for simplified wing control. However, for maximum membrane wing performance, tuning of the membrane structure to aerodynamic conditions is necessary. Bats possess an array of muscles, the plagiopatagiales proprii, embedded within the wing membrane that could serve to tune membrane stiffness, or may have alternative functions. We recorded the electromyogram from the plagiopatagiales proprii muscles of Artibeus jamaicensis, the Jamaican fruit bat, in flight at two different speeds and found that these muscles were active during downstroke. For both low- and high-speed flight, muscle activity increased between late upstroke and early downstroke and decreased at late downstroke. Thus, the array of plagiopatagiales may provide a mechanism for bats to increase wing stiffness and thereby reduce passive membrane deformation. These muscles also activate in synchrony, presumably as a means to maximize force generation, because each muscle is small and, by estimation, weak. Small differences in activation timing were observed when comparing low- and high-speed flight, which may indicate that bats modulate membrane stiffness differently depending on flight speed.

Tendon material properties vary and are interdependent among turkey hindlimb muscles

SUMMARY The material properties of a tendon affect its ability to store and return elastic energy, resist damage, provide mechanical feedback and amplify or attenuate muscle power. While the structural properties of a tendon are known to respond to a variety of stimuli, the extent to which material properties vary among individual muscles remains unclear. We studied the tendons of six different muscles in the hindlimb of Eastern wild turkeys to determine whether there was variation in elastic modulus, ultimate tensile strength and resilience. A hydraulic testing machine was used to measure tendon force during quasi-static lengthening, and a stress–strain curve was constructed. There was substantial variation in tendon material properties among different muscles. Average elastic modulus differed significantly between some tendons, and values for the six different tendons varied nearly twofold, from 829±140 to 1479±106 MPa. Tendons were stretched to failure, and the stress at failure, or ultimate tensile stress, was taken as a lower-limit estimate of tendon strength. Breaking tests for four of the tendons revealed significant variation in ultimate tensile stress, ranging from 66.83±14.34 to 112.37±9.39 MPa. Resilience, or the fraction of energy returned in cyclic length changes was generally high, and one of the four tendons tested was significantly different in resilience from the other tendons (range: 90.65±0.83 to 94.02±0.71%). An analysis of correlation between material properties revealed a positive relationship between ultimate tensile strength and elastic modulus (r2=0.79). Specifically, stiffer tendons were stronger, and we suggest that this correlation results from a constrained value of breaking strain, which did not vary significantly among tendons. This finding suggests an interdependence of material properties that may have a structural basis and may explain some adaptive responses observed in studies of tendon plasticity.

Bite force is limited by the force-length relationship of skeletal muscle in black carp, Mylopharyngodon piceus

Bite force is critical to feeding success, especially in animals that crush strong, brittle foods. Maximum bite force is typically measured as one value per individual, but the force–length relationship of skeletal muscle suggests that each individual should possess a range of gape height-specific, and, therefore, prey size-specific, bite forces. We characterized the influence of prey size on pharyngeal jaw bite force in the snail-eating black carp (Mylopharyngodon piceus, family Cyprinidae), using feeding trials on artificial prey that varied independently in size and strength. We then measured jaw-closing muscle lengths in vivo for each prey size, and then determined the force–length relationship of the same muscle in situ using tetanic stimulations. Maximum bite force was surprisingly high: the largest individual produced nearly 700 N at optimal muscle length. Bite force decreased on large and small prey, which elicited long and short muscle lengths, respectively, demonstrating that the force–length relationship of skeletal muscle results in prey size-specific bite force.

Evolution of high trophic diversity based on limited functional disparity in the feeding apparatus of marine angelfishes (f. Pomacanthidae)

The use of biting to obtain food items attached to the substratum is an ecologically widespread and important mode of feeding among aquatic vertebrates, which rarely has been studied. We did the first evolutionary analyses of morphology and motion kinematics of the feeding apparatus in Indo-Pacific members of an iconic family of biters, the marine angelfishes (f. Pomacanthidae). We found clear interspecific differences in gut morphology that clearly reflected a wide range of trophic niches. In contrast, feeding apparatus morphology appeared to be conserved. A few unusual structural innovations enabled angelfishes to protrude their jaws, close them in the protruded state, and tear food items from the substratum at a high velocity. Only one clade, the speciose pygmy angelfishes, showed functional departure from the generalized and clade-defining grab-and-tearing feeding pattern. By comparing the feeding kinematics of angelfishes with wrasses and parrotfishes (f. Labridae) we showed that grab-and-tearing is based on low kinematics disparity. Regardless of its restricted disparity, the grab-and-tearing feeding apparatus has enabled angelfishes to negotiate ecological thresholds: Given their widely different body sizes, angelfishes can access many structurally complex benthic surfaces that other biters likely are unable to exploit. From these surfaces, angelfishes can dislodge sturdy food items from their tough attachments. Angelfishes thus provide an intriguing example of a successful group that appears to have evolved considerable trophic diversity based on an unusual yet conserved feeding apparatus configuration that is characterized by limited functional disparity.

Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing

A complex sling of muscles moves and stabilizes the hyoid bone during many mammalian behaviors. One muscle in this sling, the sternohyoid, is recruited during food acquisition, processing, and swallowing, and also during nonfeeding behaviors. We used synchronous sonomicrometry and electromyography to investigate regional (intramuscular) changes in length and electromyographic (EMG) activity of the sternohyoid during swallowing in the infant pig. The simple straplike architecture of the sternohyoid led us to hypothesize that limited regional variation in length and muscle activity would be present. We found statistically significant regional differences in EMG activity, and, with respect to length dynamics, the sternohyoid did not behave homogeneously during swallowing. The midbelly region typically shortened while the anterior and posterior regions lengthened, although in a minority of swallows (12.5%) the midbelly lengthened simultaneously with the end-regions. Despite its nonpennate architecture and evolutionarily conservative innervation, the mammalian sternohyoid appears to contain previously unrecognized populations of regionally specialized motor units. It also displays differential contraction patterns, very similar to the sternohyoid of nonmammalian vertebrates.