Muscle mechanics and hydrodynamics of jet propulsion swimming in marine invertebrates

Locomotion amongst animals is widespread and diverse. Movement is of fundamental biological importance to animals, enabling them to forage, migrate, pursue prey and mate. Animals have evolved a great range of locomotor mechanisms that span huge size ranges and diversity across the animal kingdom, yet several common principles underlie most of these mechanisms, the understanding of which can help explain why certain biological locomotor systems have evolved for particular environments. Constraints on an animal’s morphological traits are bought about by body size, meaning that several aspects of locomotor performance are found to vary with body mass. Burst performance plays a crucial role in many animals lives, with the ability to accelerate and manoeuvre quickly often being essential for survival. The power available from the muscles during this type of locomotion is generally thought to decrease with increasing body size, with cycle frequency predicted to limit maximal muscle mass-specific performance. Muscle mass-specific power was measured in vivo in scallops covering a 96-fold range in body mass. Power was measured using sonomicrometry crystals to measure muscle length changes during swimming whilst pressure was simultaneously monitored within the mantle cavity. The scaling of the contractile characteristics of the adductor muscles of scallops was investigated to determine what affect the intrinsic properties of the muscle have on the scaling of muscle power output. Muscle fibre bundles were dissected and attached to a force transducer to measure force and muscle length change. Muscles were electrically stimulated via platinum plate electrodes. The scaling of twitch kinetics and the force velocity relationship were characterised in vitro. Jet propulsion via pulsed jets have been shown to be able to produce more thrust per unit of ejected fluid then an equivalent steady jet. The benefit is bought about through the production of isolated vortex rings, which entrain additional ambient fluid into the wake. There are numerous biological swimmers that use jet propulsion as their primary form of locomotion, however, their ability to be able to use vortex rings to enhance their propulsive performance has only been investigated in a few systems. Jet wake structure and swimming performance were quantified in three animals that swim by jet propulsion; scallops, Nautilus and jellyfish. The properties of the wakes were characterised using particle image velocimetry to measure the wake structure of the jets that were produced. Muscle mass-specific power output was found to decrease with increasing size in scallops. Frequency decreased with increasing size, muscle stress was found to be approximately constant whilst muscle strain decreased with increasing size in king scallops. The scaling exponents for muscle power were greater than those of the scaling of cycle frequency, suggesting that cycle frequency is not the sole determinant of the scaling of muscle power output. Muscle power output measured in vitro was also found to decrease with increasing body mass, but scaled with an exponent greater than that measured in vivo. The Vmax of the muscles decreased with increasing size, but did not scale in the same way as cycle frequency, suggesting that the intrinsic contractile properties of the muscle were not the sole determinant of cycle frequency in scallops. King scallops and Nautilus were found to produce two distinct jet modes, one in which isolated vortex rings were produced (Jet mode 1) and one which consisted of a leading vortex ring followed by a trailing jet of fluid (Jet mode 2). No differences were found in jet mode and the thrust produced from the jet, although enhanced thrust was found in king scallops producing jets at formation numbers of ~4. The wake structure of Rhizostomeae jellyfish revealed that they propel themselves via and interaction of two vortex rings that are produced as they swim. They were also found to manipulate the formation of a vortex ring that is formed as they swim, manoeuvring it to within their sub-umbrella cavity, providing them with an additional boost during swimming.