Passive stiffness of hindlimb muscles in anurans with distinct locomotor specializations

Danos, Nicole; Azizi, Emanuel

doi:10.1016/j.zool.2015.02.003

Cited by 10 publications

(7 citation statements)

References 28 publications

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“…The body may respond to perturbations differently at different times (Brown and Loeb 2000;Jindrich and Full 2002;Holmes et al 2006;Proctor and Holmes 2010). For example, many body tissues have nonlinear responses, meaning that they change stiffness at high strain compared to low strain (Danos and Azizi 2015;Porter et al 2016). Similarly, damping, or viscosity, may change with strain or strain rate .…”

Section: Introductionmentioning

confidence: 99%

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

Tytell

Carr

Danos

et al. 2018

Integrative and Comparative Biology

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Unlike most manmade machines, animals move through their world using flexible bodies and appendages, which bend due to internal muscle and body forces, and also due to forces from the environment. Fishes in particular must cope with fluid dynamic forces that not only resist their overall swimming movements but also may have unsteady flow patterns, vortices, and turbulence, many of which occur more rapidly than what the nervous system can process. Has natural selection led to mechanical properties of fish bodies and their component tissues that can respond very quickly to environmental perturbations? Here, we focus on the mechanical properties of isolated muscle tissue and of the entire intact body in the silver lamprey, Ichthyomyzon unicuspis. We developed two modified work loop protocols to determine the effect of small perturbations on the whole body and on isolated segments of muscle as a function of muscle activation and phase within the swimming cycle. First, we examined how the mechanical properties of the whole lamprey body change depending on the timing of muscle activity. Relative to passive muscle, muscle activation can modulate the effective stiffness by about two-fold and modulate the effective damping by >10-fold depending on the activation phase. Next, we performed a standard work loop test on small sections of axial musculature while adding low-amplitude sinusoidal perturbations at specific frequencies. We modeled the data using a new system identification technique based on time-periodic system analysis and harmonic transfer functions (HTFs) and used the resulting models to predict muscle function under novel conditions. We found that the effective stiffness and damping of muscle varies during the swimming cycle, and that the timing of activation can alter both the magnitude and timing of peak stiffness and damping. Moreover, the response of the isolated muscle was highly nonlinear and length dependent, but the body's response was much more linear. We applied the resulting HTFs from our experiments to explore the effect of pairs of antagonistic muscles. The results suggest that when muscles work against each other as antagonists, the combined system has weaker nonlinearities than either muscle segment alone. Together, these results begin to provide an integrative understanding of how activation timing can tune the mechanical response properties of muscles, enabling fish to swim effectively in their complex and unpredictable environment.

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Section: Introductionmentioning

confidence: 99%

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

Tytell

Carr

Danos

et al. 2018

Integrative and Comparative Biology

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“…Kassina maculata (Duméril 1853) (red-legged running frog) is a secondary walker -despite belonging to the arboreal Hyperoliidae, K. maculata uses a walking/running gait as its primary locomotor mode (Ahn et al, 2004;Danos and Azizi, 2015). However, K. maculata also climbs, burrows, swims and jumps (Loveridge, 1976;McAllister and Channing, 1983).…”

Section: Introductionmentioning

confidence: 99%

Inverse dynamic modelling of jumping in the red-legged running frogKassina maculata

Porro

Collings

Eberhard

et al. 2017

Journal of Experimental Biology

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Although the red-legged running frog, Kassina maculata, is secondarily a walker/runner, it retains the capacity for multiple locomotor modes, including jumping at a wide range of angles (nearly 70 deg). Using simultaneous hind limb kinematics and singlefoot ground reaction forces, we performed inverse dynamics analyses to calculate moment arms and torques about the hind limb joints during jumping at different angles in K. maculata. We show that forward thrust is generated primarily at the hip and ankle, while body elevation is primarily driven by the ankle. Steeper jumps are achieved by increased thrust at the hip and ankle and greater downward rotation of the distal limb segments. Because of its proximity to the GRF vector, knee posture appears to be important in controlling torque directions about this joint and, potentially, torque magnitudes at more distal joints. Other factors correlated with higher jump angles include increased body angle in the preparatory phase, faster joint openings and increased joint excursion, higher ventrally directed force, and greater acceleration and velocity. Finally, we demonstrate that jumping performance in K. maculata does not appear to be compromised by presumed adaptation to walking/ running. Our results provide new insights into how frogs engage in a wide range of locomotor behaviours and the multi-functionality of anuran limbs.

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“…Regarding the tibia fibula, the most relevant muscles to bone modelling would have been the ankle and knee extensor, plantaris longus, and ankle extensors, tibialis posticus, tibialis anticus longus, and the knee extensor, extensor cruris brevis. Plantaris longus, and ankle extensor (Gillis & Biewener, 2000), is the main motor for swimming (Richards & Clemente, 2013) as an efficient body propulsor and foot rotator (Danos & Azizi, 2015; Richards & Biewener, 2007). Therefore, strong contractions of this muscle (Richards & Biewener, 2007) would shape the bone to resist the bending throughout the bone.…”

Section: Discussionmentioning

confidence: 99%

“…These features reflect high muscle use plasticity, allowing frogs to perform different locomotion modes efficiently. In contrast, in walker frogs, the cruralis, semimembranosus and plantaris longus show lower mass and cross-sectional area than in jumper and swimmer species (Astley, 2016;Danos & Azizi, 2015). On the contrary, arboreal frogs show thinner hind limb muscles (Manzano & Lavilla, 1995) than aquatic or terrestrial ones, thus resulting in a higher whole-body mass, facilitating the jumping, climbing and manoeuvring in vertical habitats (Moen, 2019).…”

Section: Introductionmentioning

confidence: 99%

Hind limb muscles influence the architectural properties of long bones in frogs

et al. 2022

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The Mechanostat Theory states that osteocytes sense both the intensity and directionality of the strains induced by mechanical usage and modulate the bone design accordingly. In long bones, this process may adapt anterior‐posterior and lateral‐medial strength to their mechanical environment showing regional specificity. Anuran species are ideal for analyzing the muscle‐bone relationships related to the different mechanical stresses induced by their many locomotor modes and habitat uses. This work aimed to explore the relationships between indicators of the force of the most relevant muscles to locomotion and the mechanical properties of femur and tibia fibula in preserved samples of three anuran species with different habitat use (aquatic, arboreal) and locomotion modes (swimmer, jumper, walker/climber). For that purpose, we measured the anatomical cross‐sectional area of each dissected muscle and correlated it with the moments of inertia and bone strength indices. Significant, species‐specific covariations between muscle and bone parameters were observed. Pseudis platensis, the aquatic swimmer, showed the largest muscles, followed by Boana faber, the jumper and Phyllomedusa sauvagii, the walker/climber. As we expected, bigger muscles correlate with bone parameters in all the species. Nevertheless, smaller muscles also play an important role in bone design. In aquatic species, muscle interaction enhances mostly lateral bending strength throughout the femur and lateral and antero‐posterior bending strength in the tibia fibula. In the jumper species, muscles affected the femur and tibia fibula mostly in anterior‐posterior bending. In the walker/climber species, responses involving both antero‐posterior and lateral bending strengths were observed in the femur and tibia fibula. These results show that bones will be more or less resistant to lateral and antero‐posterior bending according to the different mechanical challenges of locomotion in aquatic vs. arboreal habitats. This study provides new evidence of the muscle‐bone relationships in three frog species associated with their different locomotion and habitat uses, highlighting the crucial role of muscle in determining the architectural properties of bones.

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Passive stiffness of hindlimb muscles in anurans with distinct locomotor specializations

Cited by 10 publications

References 28 publications

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

Inverse dynamic modelling of jumping in the red-legged running frogKassina maculata

Hind limb muscles influence the architectural properties of long bones in frogs

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