Fluid dynamics of odor capture by olfactory antennae
The first step in processing olfactory information, before neural filtering, is physical capture of odor molecules from the surrounding fluid. Many animals capture odors from turbulent currents or wind using antennae bearing chemosensory hairs. Much of our recent research has focused on the fluid dynamics of molecule capture by arthropod olfactory organs bearing such hairs. High-speed kinematic analyses and morphometrics of the olfactory antennules of lobsters, crabs, and stomatopods, coupled with experiments using dynamically-scaled physical models, showed that these crustaceans flick their antennules at the critical velocity at which their arrays of chemosensory hairs become leaky (i.e. at which water can flow between the hairs in the array), thus these animals take discrete water samples in space and time (i.e. they "sniff"). We found that antennule flicking has a profound effect on the flux of molecules to the chemosensory hairs, and we have been measuring how flicking antennules physically filter the information (i.e. the spatial and temporal distributions of concentration) in turbulent odor plumes in the environment.
We have also studied pheromone molecule capture by the feathery antennae of moths. We used high-speed kinematic analysis of wing beating and anemometer measurements of the air flow this produces past antennae, coupled with mathematical modeling of pheromone diffusion in the air flow between sensory hairs on the antennae. We found that wing fanning increases pheromone interception rates by two orders of magnitude because the antennae undergo a transition in their leakiness to air flow at the air velocities the wings produce.
Selected references on this topic
- Koehl, M. A. R. (1996) Small-Scale fluid dynamics of olfactory antennae. Mar. Fresh. Behav. Physiol. 27: 127-141.
- Mead, K. S., M. A. R. Koehl and M. J. O'Donnell (1999) Stomatopod sniffing: The scaling of chemosensory sensillae and flicking behavior with body size. J. Exp. Mar. Biol. Ecol. 241: 235-261.
- Loudon, C. and M. A. R. Koehl. (2000) Sniffing by a silkworm moth: Wing fanning enhances air penetration through and pheromone interception by antennae. J. Exp. Biol. 203: 2977-2990.
- Mead, K. S. and M. A. R. Koehl (2000) Stomatopod antennule design: The assymmetry, sampling efficiency, and ontogeny of olfactory flicking. J. Exp. Biol. 203: 3795-3808.
- Koehl, M. A. R. (2001) Fluid dynamics of animal appendages that capture molecules: Arthropod olfactory antennae. pp. 97-116 In, Computational Modeling in Biological Fluid Dynamics. L. Fauci and S. Gueron [eds.], IMA Series #124.
- Goldman, J. A. and M. A. R. Koehl (2001) Fluid dynamic design of lobster olfactory organs: High-speed kinematic analysis of antennule flicking by Panulirus argus. Chemical Senses 26: 385-398.
- Koehl, M. A. R. (2001) Transitions in function at low Reynolds number: Hair-bearing animal appendages. Math. Meth. Appl. Sci. 24: 1523-1532.
- Stacey, M., K. S. Mead, and M. A. R. Koehl (2002) Molecule capture by olfactory antennules: Mantis shrimp. J. Math. Biol. 44: 1-30.
- Crimaldi, J. P., M. A. R. Koehl, and J. R. Koseff (2002) Effects of the resolution and behavior of olfactory appendages on the chemical signals they intercept in a turbulent odor plume. Environ. Fluid Mech. 2: 35-63.
- Koehl, M. A. R., J. R. Koseff, J. P. Crimaldi, M. G. McCay, T. Cooper, M. B. Wiley, and P. A. Moore (2001) Lobster sniffing: Antennule design and hydrodynamic filtering of information in an odor plume. Science 294: 1948-1952.
- Mead, K. S., M. B. Wiley, M. A. R. Koehl and J. R. Koseff (2003) Fine-scale patterns of odor encounter by the antennules of mantis shrimp tracking turbulent plumes in wave-affected and unidirectional flow. J. Exp. Biol. 206: 181-193.
- Koehl, M. A. R. (2003) Physical modelling in biomechanics. Phil Trans. Roy. Soc. Lond. B 358: 1589-1596.
- Koehl, M. A. R. (2006) The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem. Senses 31: 93-105.
- Reidenbach, M. A., N. George, and M. A. R. Koehl (2008) Antennule morphology and flicking kinematics facilitate odor sampling in the spiny lobster, Panulirus argus. J. Exp. biol. 211: 2849-2858.
- Koehl, M. A. R.(2011) Hydrodynamics of sniffing by crustaceans. In: Chemical Communication in Crustaceans. T. Breithaupt and M. Theil [eds], Springer Verlag, pp. 85-102.
- Reidenbach, M.A. and M. A. R. Koehl (2011) The spatial and temporal patterns of odors sampled by lobsters and crabs in a turbulent plume. J. Exp. Biol. 214: 3138-3153.
- Schuech, R., M.T. Stacey, M. F. Barad, and M. A. R. Koehl (2011) Numerical simulations of odorant detection by biologically inspired sensory arrays. IOP Journal of Bioinspiration and Biomimetics. doi:10.1088/1748-3182/7/1/016001.
- Waldrop, L. D., M. Hann, A. Henry, A. Kim, A. Punjabi, and M. A. R. Koehl (2015) Ontogenetic changes in the olfactory antennules of the shore crab, Hemigrapsus oregonensis, maintain sniffing function during growth. Journal of the Royal Society Interface. DOI: 10.1098/rsif.2014.1077
- Waldrop, L. D. Reidenbach, M. A., and Koehl, M. A. R. (2015) Flexibility of Crab Chemosensory Sensilla Enables Flicking Antennules to Sniff. Biol. Bull. 229: 185–198.
- Waldrop, L. D. and M. A. R. Koehl (2016) Do terrestrial hermit crabs sniff? Air flow and odorant capture by flicking antennules. J. Roy. Soc. Interface 13: 20150850. doi.org/10.1098/rsif.2015.0850
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