skip to main content

Title: Compliant Substrates Disrupt Elastic Energy Storage in Jumping Tree Frogs
Abstract

Arboreal frogs navigate complex environments and face diverse mechanical properties within their physical environment. Such frogs may encounter substrates that are damped and absorb energy or are elastic and can store and release energy as the animal pushes off during take-off. When dealing with a compliant substrate, a well-coordinated jump would allow for the recovery of elastic energy stored in the substrate to amplify mechanical power, effectively adding an in-series spring to the hindlimbs. We tested the hypothesis that effective use of compliant substrates requires active changes to muscle activation and limb kinematics to recover energy from the substrate. We designed an actuated force platform, modulated with a real-time feedback controller to vary the stiffness of the substrate. We quantified the kinetics and kinematics of Cuban tree frogs (Osteopilus septentrionalis) jumping off platforms at four different stiffness conditions. In addition, we used electromyography to examine the relationship between muscle activation patterns and substrate compliance during take-off in a knee extensor (m. cruralis) and an ankle extensor (m. plantaris). We find O. septentrionalis do not modulate motor patterns in response to substrate compliance. Although not actively modulated, changes in the rate of limb extension suggest a trade-off between power amplification more » and energy recovery from the substrate. Our results suggest that compliant substrates disrupt the inertial catch mechanism that allows tree frogs to store elastic energy in the tendon, thereby slowing the rate of limb extension and increasing the duration of take-off. However, the slower rate of limb extension does provide additional time to recover more energy from the substrate. This work serves to broaden our understanding of how the intrinsic mechanical properties of a system may broaden an organism’s capacity to maintain performance when facing environmental perturbations.

« less
Authors:
 ;  ;  ;  
Publication Date:
NSF-PAR ID:
10115820
Journal Name:
Integrative and Comparative Biology
ISSN:
1540-7063
Publisher:
Oxford University Press
Sponsoring Org:
National Science Foundation
More Like this
  1. Power amplification allows animals to produce movements that exceed the physiological limits of muscle power and speed, such as the mantis shrimp’s ultrafast predatory strike and the flea’s jump. However, all known examples of nonhuman, muscle-driven power amplification involve anatomical structures that store energy from a single cycle of muscular contraction. Here, we describe a nonhuman example of external power amplification using a constructed device: the web of the triangle-weaver spider, Hyptiotes cavatus , which uses energy stored in the silk threads to actively tangle prey from afar. Hyptiotes stretches its web by tightening a separate anchor line over multiple cycles of limb motion, and then releases its hold on the anchor line when insects strike the web. Both spider and web spring forward 2 to 3 cm with a peak acceleration of up to 772.85 m/s 2 so that up to four additional adhesive capture threads contact the prey while jerking caused by the spider’s sudden stop subsequently wraps silk around the prey from all directions. Using webs as external “tools” to store energy offers substantial mechanical advantages over internal tissue-based power amplification due to the ability of Hyptiotes to load the web over multiple cycles of muscular contractionmore »and thus release more stored energy during prey capture than would be possible with muscle-driven anatomical elastic-energy systems. Elastic power amplification is an underappreciated component of silk’s function in webs and shows remarkable convergence to the fundamental mechanical advantages that led humans to engineer power-amplifying devices such as catapults and ballistae.« less
  2. Endothelial mechanobiology is a key consideration in the progression of vascular dysfunction, including atherosclerosis. However mechanistic connections between the clinically associated physical stimuli, vessel stiffness and shear stress, and how they interact to modulate plaque progression remain incompletely characterized. Vessel-chip systems are excellent candidates for modeling vascular mechanobiology as they may be engineered from the ground up, guided by the mechanical parameters present in human arteries and veins, to recapitulate key features of the vasculature. Here, we report extensive validation of a vessel-chip model of endothelial yes-associated protein (YAP) mechanobiology, a protein sensitive to both matrix stiffness and shearing forces and, importantly, implicated in atherosclerotic progression. Our model captures the established endothelial mechanoresponse, with endothelial alignment, elongation, reduction of adhesion molecules, and YAP cytoplasmic retention under high laminar shear. Conversely, we observed disturbed morphology, inflammation, and nuclear partitioning under low, high, and high oscillatory shear. Examining targets of YAP transcriptional co-activation, connective tissue growth factor (CTGF) is strongly downregulated by high laminar shear, whereas it is strongly upregulated by low shear or oscillatory flow. Ankyrin repeat domain 1 (ANKRD1) is only upregulated by high oscillatory shear. Verteporfin inhibition of YAP reduced the expression of CTGF but did not affect ANKRD1.more »Lastly, substrate stiffness modulated the endothelial shear mechanoresponse. Under high shear, softer substrates showed the lowest nuclear localization of YAP whereas stiffer substrates increased nuclear localization. Low shear strongly increased nuclear localization of YAP across stiffnesses. Together, we have validated a model of endothelial mechanobiology and describe a clinically relevant biological connection between matrix stiffness, shear stress, and endothelial activation via YAP mechanobiology.« less
  3. ABSTRACT The northern clingfish (Gobiesox maeandricus) has a suction-based adhesive disc that can stick to incredibly rough surfaces, a challenge for stiff commercial suction cups. Both clingfish discs and bioinspired suction cups have stiff cores but flexible edges that can deform to overcome surface irregularities. Compliant surfaces are common in nature and technical settings, but performance data for fish and commercial cups are gathered from stiff surfaces. We quantified the interaction between substrate compliance, surface roughness and suction performance for the northern clingfish, commercial suction cups and three biomimetic suction cups with disc rims of varying compliance. We found that all cups stick better on stiffer substrates and worse on more compliant ones, as indicated by peak stress values. On compliant substrates, surface roughness had little effect on adhesion, even for commercial cups that normally fail on hard, rough surfaces. We propose that suction performance on compliant substrates can be explained in part by effective elastic modulus, the combined elastic modulus from a cup–substrate interaction. Of all the tested cups, the biomimetic cups performed the best on compliant surfaces, highlighting their potential to be used in medical and marine geotechnical fields. Lastly, we discuss the overmolding technique used to generatemore »the bioinspired cups and how it is an important tool for studying biology.« less
  4. Studies from the past two decades have demonstrated convincingly that cells are able to sense the mechanical properties of their surroundings. Cells make major decisions in response to this mechanosensation, including decisions regarding cell migration, proliferation, survival, and differentiation. The vast majority of these studies have focused on the cellular mechanoresponse to changing substrate stiffness (or elastic modulus) and have been conducted on purely elastic substrates. In contrast, most soft tissues in the human body exhibit viscoelastic behavior; that is, they generate responsive force proportional to both the magnitude and rate of strain. While several recent studies have demonstrated that viscous effects of an underlying substrate affect cellular mechanoresponse, there is not a straightforward experimental method to probe this, particularly for investigators with little background in biomaterial fabrication. In the current work, we demonstrate that polymers comprised of differing polydimethylsiloxane (PDMS) formulations can be generated that allow for control over both the strain-dependent storage modulus and the strain rate-dependent loss modulus. These substrates requires no background in biomaterial fabrication to fabricate, are shelf-stable, and exhibit repeatable mechanical properties. Here we demonstrate that these substrates are biocompatible and exhibit similar protein adsorption characteristics regardless of mechanical properties. Finally, we develop amore »set of empirical equations that predicts the storage and loss modulus for a given blend of PDMS formulations, allowing users to tailor substrate mechanical properties to their specific needs.« less
  5. Abstract

    Many studies of the flow of energy between the body, muscles, and elastic elements highlight advantages of the storage and recovery of elastic energy. The spring-like action of structures associated with muscles allows for movements that are less costly, more powerful and safer than would be possible with contractile elements alone. But these actions also present challenges that might not be present if the pattern of energy flow were simpler, for example, if power were always applied directly from muscle to motions of the body. Muscle is under the direct control of the nervous system, and precise modulation of activity can allow for finely controlled displacement and force. Elastic structures deform under load in a predictable way, but are not under direct control, thus both displacement and the flow of energy act at the mercy of the mechanical interaction of muscle and forces associated with movement. Studies on isolated muscle-tendon units highlight the challenges of controlling such systems. A carefully tuned activation pattern is necessary for effective cycling of energy between tendon and the environment; most activation patterns lead to futile cycling of energy between tendon and muscle. In power-amplified systems, “elastic backfire” sometimes occurs, where energy loaded intomore »tendon acts to lengthen active muscles, rather than accelerate the body. Classic models of proprioception that rely on muscle spindle organs for sensing muscle and joint displacement illustrate how elastic structures might influence sensory feedback by decoupling joint movement from muscle fiber displacements. The significance of the complex flow of energy between muscles, elastic elements and the body for neuromotor control is worth exploring.

    « less