Neurophysiology and biomechanics of squid locomotion

Locomotion is the basis of many fundamental behaviors in squid and is in turn influenced by a suite of factors, including underlying physiology, environmental variation, and hydrodynamics. To study the some of the multiple facets that shape squid locomotion, I have integrated techniques across neurophysiology and biomechanics to gain a more comprehensive view of how squid move through their underwater world. This dissertation examines the complexity of jet propulsion in three different studies that reveal how squid operate near functional limits of their capabilities. Squid utilize jet propulsion immediately upon hatching, and the jet remains a crucial component of their swimming through juvenile and adult life stages. Underlying the jet are two parallel neural pathways, the giant and non-giant axon systems, that directly affect the timing and magnitude of jets produced. Whereas the giant axon system is known to give rise to strong stereotyped jets, the non-giant system produces graded mantle contractions. Although non-giant activity typically yields weaker jets, inputs from the non-giant system can summate to produce mantle contractions comparable to or exceeding those of the giant system. The role of the two neural pathways on mantle kinematics is well understood, but it is unclear how neuromuscular mechanisms influence the jet once it is expelled into the surrounding fluid. To explore the influence of the giant and non-giant systems on jet hydrodynamics in Chapter 1, I simultaneously measured neural activity, mantle contractions, and wake structure of jets produced by each neural pathway in adult squid. Jets associated with the giant axon system exhibited on average greater impulse calculated from the wake structure than those of the non-giant system. Furthermore, giant axon jets produced a tightly clustered range of impulse values, whereas resultant output from the non-giant system appeared more flexible. In rare instances, non-giant activity was associated with impulse four times as great as that of the giant system. This suggests that the influence of the neural pathways on mantle kinematics can extend to hydrodynamic characteristics of the jet as well. Like adult squid, newly hatched squid paralarvae must also successfully produce jets, but they contend with and utilize a fluid environment with both viscous and inertial forces. Whereas adult squid are large enough take advantage of inertia and coast when jetting through seawater, viscous diffusion can substantially alter jet wake structure for a millimeter-scale paralarva. By artificially increasing the viscosity of seawater in Chapter 2, I empirically show how a growing dominance of viscous forces disrupts the wake structure of paralarval jets such that energy and momentum quickly dissipate and the jet's thrust is substantially reduced. With high enough viscous forces, mantle contractions do not generate movement and jet propulsion no longer is an effective means of locomotion. A dynamically similar scenario in seawater would require a paralarva to be smaller than any observed size in nature, thus implying viscous forces may play a role in hydrodynamically constraining squid size at hatch. Finally, Chapter 3 examines how squid's highly dynamic surrounding environment can impact locomotion. The thermal dependence of the jet and its neuromuscular mechanisms have been well-characterized, but the impact of low oxygen that often accompanies cold waters in a squid's natural habitat remain unexplored. By measuring the squid's powerful jet-propelled escape response mediated by the giant axon system, I find that giant axon activity becomes reduced and delayed under severe hypoxia, thus similarly hindering the escape jet. However, the response is able to fully recover once oxygen levels increase, suggesting that it is robust against the range of dissolved oxygen observed in the field.

Keywords: Biology.
Advisor: Denny Mark W.
Gilly William 
Goldbogen Jeremy