Elastic Recoil Mechanism Research Articles

Parallel And Divergent Morphological Adaptations Underlying The Evolution of Jumping Ability in Ants.

Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during jump, however, varies across these genera. It is unknown what morphological adaptations underlie such behaviors and whether jumping in ants is solely driven directly by muscle contraction or additionally relies on elastic recoil mechanism. We investigated the morphological adaptations for jumping behavior by comparing differences in the locomotory musculature between jumping and non-jumping relatives using X-ray micro-CT and 3D morphometrics. We found that the size-specific volumes of the trochanter depressor muscle (scm6) of the middle and hind legs are 3-5 times larger in jumping ants, and that one coxal remotor muscle (scm2) is reduced in volume in the middle and/or hind legs. Notably, the enlargement in the volume of other muscle groups is directly linked to the legs or body parts engaged during the jump. Furthermore, a direct comparison of the muscle architecture revealed two significant differences between jumping vs. non-jumping ants: First, the relative Physiological Cross-Sectional Area (PCSA) of the trochanter depressor muscles of all three legs were larger in jumping ants, except in the front legs of Odontomachus rixosus and Myrmecia nigrocincta; second, the relative muscle fiber length was shorter in jumping ants compared to non-jumping counterparts, except in the front legs of O. rixosus and M. nigrocincta. These results suggest that the difference in relative muscle volume in jumping ants is largely invested in the area (PCSA), and not in fiber length. There was no clear difference in the pennation angle between jumping and non-jumping ants. Additionally, we report that the hind leg length relative to body length was longer in jumping ants. Based on direct comparison of the observed vs. possible work and power output during jumps, we surmise that direct muscle contractions suffice to explain jumping performance in three species, except for O. rixosus, where the lack of data on jumping performance prevents us from drawing definitive conclusions for this particular species. We suggest that increased investment in jumping-relevant musculature is a primary morphological adaptation that separates jumping from non-jumping ants. These results elucidate the common and idiosyncratic morphological changes underlying this rare adaptation in ants. まとぅみ (Okinawan language-Uchinaaguchi) (Japanese) РЕЗЮМЕ (Kazakh) ZUSAMMENFASSUNG (German).

A physical model of mantis shrimp for exploring the dynamics of ultrafast systems

Efficient and effective generation of high-acceleration movement in biology requires a process to control energy flow and amplify mechanical power from power density-limited muscle. Until recently, this ability was exclusive to ultrafast, small organisms, and this process was largely ascribed to the high mechanical power density of small elastic recoil mechanisms. In several ultrafast organisms, linkages suddenly initiate rotation when they overcenter and reverse torque; this process mediates the release of stored elastic energy and enhances the mechanical power output of extremely fast, spring-actuated systems. Here we report the discovery of linkage dynamics and geometric latching that reveals how organisms and synthetic systems generate extremely high-acceleration, short-duration movements. Through synergistic analyses of mantis shrimp strikes, a synthetic mantis shrimp robot, and a dynamic mathematical model, we discover that linkages can exhibit distinct dynamic phases that control energy transfer from stored elastic energy to ultrafast movement. These design principles are embodied in a 1.5-g mantis shrimp scale mechanism capable of striking velocities over 26 m [Formula: see text] in air and 5 m [Formula: see text] in water. The physical, mathematical, and biological datasets establish latching mechanics with four temporal phases and identify a nondimensional performance metric to analyze potential energy transfer. These temporal phases enable control of an extreme cascade of mechanical power amplification. Linkage dynamics and temporal phase characteristics are easily adjusted through linkage design in robotic and mathematical systems and provide a framework to understand the function of linkages and latches in biological systems.

Temperature effects on the jumping performance of house crickets.

Insect jumping and other explosive animal movements often make use of elastic-recoil mechanisms to enhance performance. These mechanisms circumvent the intrinsic rate limitations on muscle shortening, allowing for greater power production as well as thermal robustness of the associated movements. Here we examine the performance and temperature effects on jumping in the house cricket, Acheta domesticus, using high-speed imaging and inverse dynamics analysis. We find that adult house crickets jumped with greater performance than would be possible using direct muscle shortening, generating a peak power of over 2000 W/kg of muscle mass and maintaining high performance across the entire tested range of body temperatures (12-32°C). Performance declined at the lowest temperature (12°C), yet jump power still exceeds available muscle power. These results reveal that Acheta domesticus makes use of an elastic-recoil mechanism that enhances both the performance and thermal robustness of jumping.

Evolution of a high-performance and functionally robust musculoskeletal system in salamanders

The evolution of ballistic tongue projection in plethodontid salamanders-a high-performance and thermally robust musculoskeletal system-is ideal for examining how the components required for extreme performance in animal movement are assembled in evolution. Our comparative data on whole-organism performance measured across a range of temperatures and the musculoskeletal morphology of the tongue apparatus were examined in a phylogenetic framework and combined with data on muscle contractile physiology and neural control. Our analysis reveals that relatively minor evolutionary changes in morphology and neural control have transformed a muscle-powered system with modest performance and high thermal sensitivity into a spring-powered system with extreme performance and functional robustness in the face of evolutionarily conserved muscle contractile physiology. Furthermore, these changes have occurred in parallel in both major clades of this largest family of salamanders. We also find that high-performance tongue projection that exceeds available muscle power and thermal robustness of performance coevolve, both being emergent properties of the same elastic-recoil mechanism. Among the taxa examined, we find muscle-powered and fully fledged elastic systems with enormous performance differences, but no intermediate forms, suggesting that incipient elastic mechanisms do not persist in evolutionary time. A growing body of data from other elastic systems suggests that similar coevolution of traits may be found in other ectothermic animals with high performance, particularly those for which thermoregulation is challenging or ecologically costly.

Modeling the Determinants of Mechanical Advantage During Jumping: Consequences for Spring- and Muscle-Driven Movement.

Systems powered by elastic recoil need a latch to prevent motion while a spring is loaded but allow motion during spring recoil. Some jumping animals that rely on elastic recoil use the increasing mechanical advantage of limb extensor muscles to accomplish latching. We examined the ways in which limb morphology affects latching and the resulting performance of an elastic-recoil mechanism. Additionally, because increasing mechanical advantage is a consequence of limb extension that may be found in many systems, we examined the mechanical consequences for muscle in the absence of elastic elements. By simulating muscle contractions against a simplified model of an extending limb, we found that increasing mechanical advantage can limit the work done by muscle by accelerating muscle shortening during limb extension. The inclusion of a series elastic element dramatically improves mechanical output by allowing for additional muscle work that is stored and released from the spring. This suggests that elastic recoil may be beneficial for more animals than expected when assuming peak isotonic power output from muscle during jumping. The mechanical output of elastic recoil depends on limb morphology; long limbs moving small loads maximize total work, but it is done at a low power, whereas shorter limbs moving larger loads do less work at a higher power. This work-power trade-off of limb morphology is true with or without an elastic element. Systems with relatively short limbs may have performance that is robust to variable conditions such as body mass or muscle activation, while long-limbed systems risk complete failure with relatively minor perturbations. Finally, a changing mechanical advantage latch allows for muscle work to be done simultaneously with spring recoil, changing the predictions for spring mechanical properties. Overall, the design constraints revealed by considering the mechanics of this particular latch will inform our understanding of the evolution of elastic-recoil mechanisms and our attempts to engineer similar systems.

Planthopper bugs use a fast, cyclic elastic recoil mechanism for effective vibrational communication at small body size.

Vibrations through substrates are an important source of information for diverse organisms, from nematodes to elephants. The fundamental challenge for small animals using vibrational communication is to move their limited mass fast enough to provide sufficient kinetic energy for effective information transfer through the substrate whilst optimising energy efficiency over repeated cycles. Here, we describe a vibratory organ found across a commercially important group of plant-feeding insects, the planthoppers (Hemiptera: Fulgoromorpha). This elastic recoil snapping organ generates substrate-borne broadband vibrations using fast, cyclical abdominal motion that transfers kinetic energy to the substrate through the legs. Elastic potential energy is stored and released twice using two different latched energy-storage mechanisms, each utilising a different form of elastic recoil to increase the speed of motion. Comparison to the acoustic tymbal organ of cicadas (Hemiptera: Cicadomorpha) reveals functional convergence in their use of elastic mechanisms to increase the efficacy of mechanical communication.

Ballistic tongue projection in a miniaturized salamander.

Miniaturization of body size is often accompanied by peculiarities in morphology that can have functional consequences. We examined the feeding behavior and morphology of the miniaturized plethodontid salamander Thorius, one of the smallest vertebrates, to determine if its performance and biomechanics differ from those of its larger relatives. High-speed imaging and dynamics analysis of feeding at a range of temperatures show that tongue projection in Thorius macdougalli is ballistic and achieves accelerations of up to 600 G with low thermal sensitivity, indicating that tongue projection is powered by an elastic-recoil mechanism. Preceding ballistic projection is an unusual preparatory phase of tongue protrusion, which, like tongue retraction, shows lower performance and higher thermal sensitivity that are indicative of movement being powered directly by muscle shortening. The variability of tongue-projection kinematics and dynamics is comparable to larger ballistic-tongued plethodontids and reveals that Thorius is capable of modulating its tongue movements in response to prey distance. Morphological examination revealed that T. macdougalli possesses a reduced number of myofibers in the tongue muscles, a large projector muscle mass relative to tongue mass, and an unusual folding of the tongue skeleton, compared with larger relatives. Nonetheless, T. macdougalli retains the elaborated collagen aponeuroses in the projector muscle that store elastic energy and a tongue skeleton that is free of direct myofiber insertion, two features that appear to be essential for ballistic tongue projection in salamanders.

Movements of vastly different performance have similar underlying muscle physiology.

Many animals use elastic recoil mechanisms to power extreme movements, achieving levels of performance that would not be possible using muscle power alone. Contractile performance of vertebrate muscle depends strongly on temperature, but the release of energy from elastic structures is far less thermally dependent, thus elastic recoil confers thermal robustness to whole-animal performance. Here we explore the role that muscle contractile properties play in the differences in performance and thermal robustness between elastic and non-elastic systems by examining muscle from two species of plethodontid salamanders that use elastically powered tongue projection to capture prey and one that uses non-elastic tongue projection. In species with elastic mechanisms, tongue projection is characterized by higher mechanical power output and thermal robustness compared with tongue projection of closely related genera with non-elastic mechanisms. In vitro and in situ muscle experiments reveal that species differ in their muscle contractile properties, but these patterns do not predict the performance differences between elastic and non-elastic tongue projection. Overall, salamander tongue muscles are similar to other vertebrate muscles in contractile performance and thermal sensitivity. We conclude that changes in the tongue-projection mechanism, specifically the elaboration of elastic structures, are responsible for high performance and thermal robustness in species with elastic tongue projection. This suggests that the evolution of high-performance and thermally robust elastic recoil mechanisms can occur via relatively simple changes to morphology, while muscle contractile properties remain relatively unchanged.

Effects of temperature and force requirements on muscle work and power output.

Performance of muscle-powered movements depends on temperature through its effects on muscle contractile properties. In vitro stimulation of Cuban treefrog (Osteopilus septentrionalis) plantaris muscles reveals that interactions between force and temperature affect the mechanical work of muscle. At low temperatures (9-17°C), muscle work depends on temperature when shortening at any force, and temperature effects are greater at higher forces. At warmer temperatures (13-21°C), muscle work depends on temperature when shortening with intermediate and high forces (≥30% peak isometric tetanic force). Shortening velocity is most strongly affected by temperature at low temperatures and high forces. Power is also most strongly affected at low temperature intervals, but this effect is minimized at intermediate forces. Effects of temperature on muscle force explain these interactions; force production decreases at lower temperatures, increasing the challenge of moving a constant force relative to the muscle's capacity. These results suggest that animal performance that requires muscles to do work with low forces relative to a muscle's maximum force production will be robust to temperature changes, and this effect should be true whether muscle acts directly or through elastic-recoil mechanisms and whether force is prescribed (i.e. internal) or variable (i.e. external). Conversely, performance requiring muscles to shorten with relatively large forces is expected to be more sensitive to temperature changes.

Extreme Performance and Functional Robustness of Movement are Linked to Muscle Architecture: Comparing Elastic and Nonelastic Feeding Movements in Salamanders

Muscle-powered movements are limited by the contractile properties of muscles and are sensitive to temperature changes. Elastic-recoil mechanisms can both increase performance and mitigate the effects of temperature on performance. Here, we compare feeding movements in two species of plethodontid salamanders, Bolitoglossa franklini and Desmognathus quadramaculatus, across a range of body temperatures (5-25°C) to better understand the mechanism of elastically powered, thermally robust movements. Bolitoglossa exhibited ballistic, elastically powered tongue projection with a maximum muscle mass specific power of 4,642 W kg(-1) while Desmognathus demonstrated nonballistic, muscle-powered tongue projection with a maximum power of 359 W kg(-1) . Tongue-projection performance in Bolitoglossa was more thermally robust than that of Desmognathus, especially below 15°C. The improved performance and thermal robustness of Bolitoglossa was associated with morphological changes in the projector muscle, including elaborated collagen aponeuroses and the absence of myofibers attaching directly to the tongue skeleton. The elongated aponeuroses likely increase the capacity for elastic energy storage, and the lack of myofibers inserting on the tongue skeleton permits ballistic projection. These results suggest that relatively simple changes in myofiber architecture and the amount of connective tissue can improve the performance and functional robustness of movements in the face of environmental challenges such as variable temperature.

Thermal sensitivity of motor control of muscle-powered versus elastically powered tongue projection in salamanders

Elastic-recoil mechanisms can improve organismal performance and circumvent the thermal limitations of muscle contraction, yet they require the appropriate motor control to operate. We compare muscle activity during tongue projection in salamanders with elastically powered, ballistic projection with activity of those with muscle-powered, non-ballistic projection across a range of temperatures to understand how motor control is integrated with elastically powered movements, and how this integration contributes to reduced thermal sensitivity. Species with ballistic tongue projection activated and deactivated their projector muscles significantly earlier than non-ballistic species, in a pattern consistent with a mechanism in which the muscle strains elastic tissue that subsequently recoils to power projection. Tongue projection was more thermally robust in ballistic species, but in both ballistic and non-ballistic species the projector muscles were activated earlier and for longer as temperature decreased. The retractor muscles showed a pattern similar to that of the projector muscles, but declined in a similar manner in the two groups. Muscle activity intensity also decreased at low temperatures in both groups, revealing that compensatory muscle activation does not account for the improved thermal robustness in ballistic species. Thus, relatively minor shifts in motor patterns accompanying morphological changes such as increased elastic tissue are sufficient to improve performance and decrease its thermal sensitivity without specialization of muscle contractile physiology.

Dynamics and thermal sensitivity of ballistic and non-ballistic feeding in salamanders.

Low temperature reduces the performance of muscle-powered movements, but in movements powered by elastic recoil mechanisms, this effect can be mitigated and performance can be increased. To better understand the morphological basis of high performance and thermal robustness of elastically powered movements, we compared feeding dynamics at a range of temperatures (5-25°C) in two species of terrestrial plethodontid salamanders, Plethodon metcalfi and Ensatina eschscholtzii, which differ in tongue muscle architecture and the mechanism of tongue projection. We found that Ensatina is capable of ballistic projection with a mean muscle mass-specific power of 2100 W kg(-1), revealing an elastic mechanism. Plethodon, in contrast, projected its tongue non-ballistically with a mean power of only 18 W kg(-1), indicating it is muscle powered. Ensatina projected its tongue significantly farther than Plethodon and with dynamics that had significantly lower thermal sensitivity at temperatures below 15°C. These performance differences were correlated with morphological differences, namely elongated collagenous aponeuroses in the projector muscle of Ensatina as compared with Plethodon, which are likely the site of energy storage, and the absence in Ensatina of projector muscle fibers attaching to the tongue skeleton that allows projection to be truly ballistic. These findings demonstrate that, in these otherwise similar species, the presence in one species of elaborated connective tissue in series with myofibers confers not only 10-fold greater absolute performance but also greater thermal robustness of performance. We conclude that changes in muscle and connective tissue architecture are sufficient to alter significantly the mechanics, performance and thermal robustness of musculoskeletal systems.

Cold‐blooded snipers: thermal independence of ballistic tongue projection in the salamander Hydromantes platycephalus

Plethodontid salamanders of the genus Hydromantes capture prey using the most extreme tongue projection among salamanders, and can shoot the tongue a distance of 80% of body length in less than 20 msec. The tongue skeleton is projected from the body via an elastic-recoil mechanism that decouples muscle contraction from tongue projection, amplifying muscle power tenfold. We tested the hypothesis that the elastic-recoil mechanism also endows tongue projection with low thermal dependence by examining the kinematics and dynamics of tongue projection in Hydromantes platycephalus over a range of body temperatures (2-24°C). We found that H. platycephalus maintained tongue-projection performance over the tested temperature range and that tongue projection showed thermal independence (Q(10) values of 0.94-1.04) of all performance parameters including projection distance, average velocity, and peak instantaneous values of velocity, acceleration, and power. Nonelastic, muscle-powered tongue retraction, in contrast, responded to temperature changes significantly differently than elastic tongue projection; performance parameters of retraction displayed thermal dependence typical of muscle-powered movement (Q(10) values of 1.63-4.97). These results reveal that the elastic-recoil mechanism liberates tongue projection from the effects of temperature on muscle contractile rates. We suggest that relative thermal independence is a general characteristic of elastic-recoil mechanisms and may promote the evolution of these mechanisms in ectothermic animals.

Ballistic tongue projection in chameleons maintains high performance at low temperature

Environmental temperature impacts the physical activity and ecology of ectothermic animals through its effects on muscle contractile physiology. Sprinting, swimming, and jumping performance of ectotherms decreases by at least 33% over a 10 degrees C drop, accompanied by a similar decline in muscle power. We propose that ballistic movements that are powered by recoil of elastic tissues are less thermally dependent than movements that rely on direct muscular power. We found that an elastically powered movement, ballistic tongue projection in chameleons, maintains high performance over a 20 degrees C range. Peak velocity and power decline by only 10%-19% with a 10 degrees C drop, compared to >42% for nonelastic, muscle-powered tongue retraction. These results indicate that the elastic recoil mechanism circumvents the constraints that low temperature imposes on muscle rate properties and thereby reduces the thermal dependence of tongue projection. We propose that organisms that use elastic recoil mechanisms for ecologically important movements such as feeding and locomotion may benefit from an expanded thermal niche.

Suction is kid's play: extremely fast suction in newborn seahorses

Ongoing anatomical development typically results in a gradual maturation of the feeding movements from larval to adult fishes. Adult seahorses are known to capture prey by rotating their long-snouted head extremely quickly towards prey, followed by powerful suction. This type of suction is powered by elastic recoil and requires very precise coordination of the movements of the associated feeding structures, making it an all-or-none phenomenon. Here, we show that newborn Hippocampus reidi are able to successfully feed using an extremely rapid and powerful snout rotation combined with a high-volume suction, surpassing that observed in adult seahorses. An inverse dynamic analysis shows that an elastic recoil mechanism is also used to power head rotation in newborn H. reidi. This illustrates how extreme levels of performance in highly complex musculoskeletal systems can be present at birth given a delayed birth and rapid development of functionally important structures. The fact that the head skeleton of newborn seahorses is still largely cartilaginous may not be problematic because the hydrodynamic stress on the rotating snout appeared considerably lower than in adult syngnathids.

Starling's Law and Albumin Therapy-Reply

The ongoing controversy over the relative merits of albumin vs large volumes of crystalloid solution as replacement for effective plasma volume has raged for many decades. Evidence can be cited by proponents of each type of solution. Indeed, the symposium which served as the basis for my communication, carefully presented both sides of this controversy. Although Starling's law of fluid movement across a semipermeable membrane does not fit all experimental conditions, it still remains the keystone for the consideration of movement in and out of the vascular space in isolated organs or extremities. In addition to these interrelating hydrostatic and colloid osmotic pressures on the two sides of a membrane, it is necessary to invoke multiple additional forces. As clearly outlined in the review, these include tissue compliance, rates of lymph flow, changes in capillary permeability, and an intrinsic elastic recoil mechanism of connectivetissue mucopolysaccharides that exhibit inhibition