Odorant transport in a hagfish

Todor G. Cross, Olivia C. Mayo, Graham Martin, Matthew P. Cross, David K. Ludlow, Katharine Fraser, Jonathan Cox

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Abstract

Odorant transport is of fundamental and applied importance. Using computational simulations, we studied odorant transport in an anatomically accurate model of the nasal passage of a hagfish (probably Eptatretus stoutii). We found that ambient water is sampled widely, with a significant ventral element. Additionally, there is a bilateral element to olfactory flow, which enters the single nostril in two narrow, laminar streams that are then split prior to the nasal chamber by the anterior edge of the central olfactory lamella. An appendage on this lamella directs a small portion (10–14%) of the overall nasal flow to the olfactory sensory channels. Much of the remaining flow is diverted away from the sensory channels by two peripheral channels. The anterior edge of the central olfactory lamella, together with a jet-impingement mechanism, disperses flow over the olfactory surfaces. Diffusion of odorant from bulk water to the olfactory surfaces is facilitated by the large surface area:volume ratio of the sensory channels, and by a resistance-based hydrodynamic mechanism that leads to long residence times (up to 4.5 s) in the sensory channels. With increasing volumetric flow rate, the rate of odorant transfer to the olfactory surfaces increases, but the efficiency of odorant uptake decreases, falling in the range 2–6%. Odorant flux decreases caudally across the olfactory surfaces, suggesting in vivo a preponderance of olfactory sensory neurons on the anterior part of each olfactory surface. We conclude that the hagfish has a subtle anatomy for locating and capturing odorant molecules.
Original languageEnglish
Article number111711
Number of pages18
JournalComparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology
Volume297
Early online date25 Jul 2024
DOIs
Publication statusE-pub ahead of print - 25 Jul 2024

Data Availability Statement

Data will be made available on request. Stereolithography models are available at Mendeley Data, v1, 10.17632/j2ckn898jc.1.

Acknowledgements

We thank: Nick Brice, Ellie Catlin, David Elkins, Paul Frith, Adam Holmes, Jeremy Hunt, Phil Jones, Xavier Mear, James Maclaine, George Maxted, Olivier Morton, George Oates, Steve Parker, Sam Quilter and Koen van Mierlo for technical assistance; Philip Donoghue, Matthew Wills and Zhijin Wang for helpful discussions; Richie Gill for use of ScanIP; Ogle Models for 3D printing; Kevin Webb and Nic Delves-Broughton for photography; and three anonymous reviewers for their valuable suggestions.

Funding

This work was supported by the University of Bath.

FundersFunder number
University of Bath

    Keywords

    • Hagfish
    • Lamprey
    • Microfluidic devices
    • Navigation
    • Stereo olfaction

    ASJC Scopus subject areas

    • Biochemistry
    • Physiology
    • Aquatic Science
    • Animal Science and Zoology
    • Molecular Biology

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