The Hydrodynamics and Transport Phenomena of Olfaction in the Hammerhead Shark (sphyrna tudes): Implications for Bio-inspired Chemical Sensing

Open Access
Author:
Rygg, Alex Dale
Graduate Program:
Mechanical Engineering
Degree:
Doctor of Philosophy
Document Type:
Dissertation
Date of Defense:
April 29, 2014
Committee Members:
  • Brent Craven, Dissertation Advisor
  • Brent Craven, Committee Chair
  • Eric Paterson, Committee Chair
  • John Michael Cimbala, Committee Member
  • Robert Francis Kunz, Committee Member
  • Gary Stuart Settles, Committee Member
  • Adrianus C Van Duin, Committee Member
Keywords:
  • Olfaction
  • Computational Fluid Dynamics
  • Mass Transport
  • Chemical Sensing
  • Hammerhead Shark
Abstract:
Fish rely on a number of physiological senses for survival, with olfaction (the sense of smell) playing an important role in navigation, procreation, and the detection of food. Out of the vast diversity of fish species, sharks are thought to have a particularly acute sense of smell, and it is well known that hammerhead sharks have several morphological advantages for olfaction due to their unique head shape. The functional significance of this morphology has been studied to some extent, but the detailed hydrodynamics and odorant transport phenomena related to olfaction have not been thoroughly investigated in any fish. Since odorant transport from the aquatic environment to the sensory epithelium is the first critical step in olfaction, a proper understanding of olfactory function in fish is important. The objective of this study is to expand on the current knowledge of underwater olfaction by elucidating the hydrodynamics and odorant transport phenomena of olfaction in the hammerhead shark. An anatomically accurate, three-dimensional model of the head and olfactory organ of a cadaver hammerhead shark (Sphyrna tudes) specimen is reconstructed from micro-CT and MRI scans. Using this model, computational fluid dynamics simulations are carried out to investigate the hydrodynamics in the nasal region of the shark. Molecular dynamics simulations are used to calculate water/mucus partition coefficients for four underwater feeding stimulants. The partition coefficients are then utilized in mass transport simulations of odorant deposition in the hammerhead olfactory organ. Finally, a theoretical comparison of olfaction in aquatic and terrestrial species is presented, which is used to elucidate bio-inspired design principles for artificial chemical sensing in both water and air. The hydrodynamics results reveal that flow is induced through the hammerhead olfactory organ via a ram ventilation mechanism as the shark swims. The major nasal groove, which runs along the leading edge of the cephalofoil, is shown to facilitate sampling of a large spatial extent by directing oncoming flow towards the incurrent nostril. Additionally, several internal and external morphological features appear to serve as flow regulation mechanisms to limit flow speeds through the sensory channels, which may protect the delicate internal structures of the olfactory organ from otherwise high flow rates incurred by sampling a larger area. Molecular dynamics simulations reveal that the variation of seawater/mucus odorant partition coefficients is approximately one order of magnitude, in stark contrast to air/mucus odorant partition coefficients that can span up to six orders of magnitude. This limited range of underwater partition coefficients is shown to preclude appreciable chromatographic odorant separation along the sensory epithelium, as demonstrated in mass transport simulations of odorant deposition in the hammerhead olfactory organ. Thus, olfaction in fish appears to be fundamentally distinct from olfaction in air-breathing animals. A theoretical comparison of olfaction in aquatic and terrestrial species by means of dimensional analysis demonstrates that odorant uptake by the sensory epithelium of the hammerhead shark is more efficient than odorant uptake in the olfactory region of the canine, a keen-scented terrestrial animal, for comparable odorants. Phenomenologically, it appears that this is due to an increased nondimensional odorant permeability and nondimensional residence time in the olfactory organ of the hammerhead shark. The present results contribute to an improved understanding of olfaction in the hammerhead shark (Sphyrna tudes), and fish in general. Further, the results of this study have several important implications regarding bio-inspired chemical sensing in both water and air that are described in detail.