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50 Biomimetics: Biologically Inspired Technologies

parallel for a given muscle length and volume is much larger than what could be obtained with a
parallel fibered muscle. Clearly, pennate muscles are built for force. Examples of pennate muscles
are the calf muscles of humans (whose main function is to provide enough force to allow storage of
elastic energy in the Achilles tendon) and the claw closer muscles of crabs. Interestingly, the latter
uses both sarcomere (long sarcomeres) and muscle (pennation) design to generate as much grip
force as possible. This may not come as a surprise when one considers the tough shells a crab has to
crack. For the invertebrates with their exoskeletons, the pennate muscle design gives one additional
advantage. Jan Swammerdam discovered in 1737 that muscles remain constant in their volume
during contraction, a fact that falsified the then prevailing hypothesis that contraction came about
by a change in muscle volume. For a parallel-fibered muscle, the requirement of constant volume
means that the muscle must become thicker when contracting. This can be disadvantageous when
you are trapped in an exoskeleton. Pennate muscles offer the solution to this problem. Their fibers
rotate when they shorten, thereby making volume available for the thickening fibers without
changing the width of the muscle (Vogel, 2002).

2.5 MUSCLE ADAPTATION

Once a muscle has formed and its basic morphological design is set, there still is room for
remodeling. The ability to adapt in response to changes in functional demands sets living tissues
apart from their engineered counterparts. Muscles grow during development, they remodel in
response to use and disuse, and they are able to repair themselves after an injury. Fully grown
muscles still posses the ability to more than double their size by increasing either their physiological
cross-sectional area (PCSA) or their length. This is achieved by increasing muscle fiber size by
adding sarcomeres in parallel or in series, but not by increasing the number of muscle fibers. The
first signs of muscle adaptation occur within hours and adaptation can be completed within days
(Shah et al., 2001). It is not known whether adaptation involves alterations in sarcomere design.
Whether a muscle adapts by parallel or serial addition of sarcomeres is determined by the
functional demands. In strength training where the muscle is subjected to high loads, the adaptation
will involve addition of parallel sarcomeres to reduce the load on the individual contractile units
(Russell et al., 2000). This mechanism may be responsible for a more than twofold strength gain of
the muscle. Alternatively, when an animal grows or when it starts using its limbs in new body
configurations, the muscle will start adding sarcomeres in series. This mechanism can be respon-
sible for length changes of the muscle of up to 27% (Shah et al., 2001). There are a number of
theories on the mechanism for length adaptation of the muscle. Some studies have provided
evidence that a muscle strives to have its optimal muscle length at the most prevalent joint position
(Williams and Goldspink, 1973; Burkholder and Lieber, 1998), while others have argued that
maintenance of adequate joint excursion is the most important trigger (Koh and Herzog, 1998).
Another theory is that muscles adapt their length to prevent injury. In severely injured muscles,
entire muscle fibers are replaced, however, in mild injury involving local lesions to sarcomeres just
the damaged sarcomere are replaced. Muscle responds to injury with overcompensation probably
as a safety precaution to future incidents. Lynn et al. (1998) have shown that injury induced by
eccentric contractions results in addition of serial sarcomeres. The consequence of this adaptation is
that the recovered muscle will operate at the ascending limb of its length–tension relationship,
where it is less prone to lengthening induced injury. It is conceivable that all three mechanisms co-
exist, but the length at which the muscle operates determines their action. It has been observed that
the operating range of different muscles is scattered over the entire functional length range, some
muscles work on the ascending limb and others on the descending limb (Burkholder and Lieber,
2001; Lieber and Burkholder, 2000). This is also reflected in the observation that muscles within a
single anatomical group display different adaptations that are triggered by functional demands
(Savelberg and Meijer, 2003).