Antennule morphology and flicking kinematics facilitate odor sampling by the spiny lobster, Panulirus argus

Abstract

SUMMARYMany arthropod olfactory appendages bear arrays of hair-like chemosensory sensillae. Odor molecules in the fluid around the animal must reach the surfaces of those hairs to be sensed. We used the lateral flagellum of the olfactory antennule of the spiny lobster, Panulirus argus, as a system to study how the morphology, orientation, and motion of sensilla-bearing appendages affects the small-scale water flow within the hair array. We tested whether antennule flicking enables lobsters to take discrete odor samples by measuring flow fields through an aesthetasc array on a dynamically scaled physical model of a P. argus antennule. Particle image velocimetry revealed that the magnitude and duration of velocity through the aesthetasc array during the rapid flick downstroke is just enough to allow complete replacement of the fluid entrained within the hair array. The complex zig-zag arrangement of aesthetascs hairs, combined with their offset orientation along the antennule, generates flow velocities that are uniform along the length of the hairs. This increases fluid exchange during the flick and reduces the boundary layer thickness surrounding the hairs. The return stroke occurs at about a quarter the speed of the flick, but the velocity of the fluid between the aesthetascs is approximately 25 times slower. The retained fluid during the return stroke remains virtually unstirred and sufficient time occurs for odor molecules to diffuse to aesthetasc surfaces.

Identified antennular near-field receptors trigger reflex flicking in the crayfish

“…Fluid flow around these structures is therefore laminar, and the fluid boundary layer accompanying each of the aesthetasc sensilla will accordingly be relatively thick, except when the lateral flagella are flicked through the fluid medium at a high enough velocity to dynamically shed some or most of it. By reducing the thickness of the boundary layer around individual aesthetascs, flicking promotes access of odorant-laden fluid to the cuticular surface of the sensilla (Cheer and Koehl, 1987;Goldman and Koehl, 2001;Koehl et al, 2001;Reidenbach et al, 2008;Mellon and Reidenbach, 2011). This behavior thereby improves the diffusional exposure of olfactory receptor neuron dendrites within the aesthetascs to odorants embedded in the fluid column.…”

Smelling, feeling, tasting and touching: behavioral and neural integration of antennular chemosensory and mechanosensory inputs in the crayfish

“…The moment-to-moment detection of hydrodynamic discontinuities may therefore be of crucial importance in odorant capture. At the same time, antennular flicking enhances the detection of dissolved odorants by shedding, or at least by decreasing, the fluid boundary layer around the individual aesthetasc sensilla, thereby enhancing their exposure to novel water samples and their imbedded chemical agents through molecular diffusion (Reidenbach et al, 2008;Mellon and Reidenbach, 2011). Turbulent eddy fronts within the water column are therefore cues to the possibility of novel odorant exposure, and they trigger antennular flicking.…”

The spatial and temporal patterns of odors sampled by lobsters and crabs in a turbulent plume

“…During the rapid downstroke of the antennule flick of lobsters and crabs, water flows between the aesthetascs (Mead and Koehl, 2000;Reidenbach et al, 2008;Koehl, 2011), but does not appreciably alter the filamentous structure of odors within the ambient flow Koehl, 2006;Koehl, 2011;Reidenbach et al, 2008). During the slower return stroke and during the stationary pause between flicks, water does not flow through the aesthetasc array (Mead and Koehl, 2000;Reidenbach et al, 2008;Koehl, 2011).…”

“…During the rapid downstroke of the antennule flick of lobsters and crabs, water flows between the aesthetascs (Mead and Koehl, 2000;Reidenbach et al, 2008;Koehl, 2011), but does not appreciably alter the filamentous structure of odors within the ambient flow Koehl, 2006;Koehl, 2011;Reidenbach et al, 2008). During the slower return stroke and during the stationary pause between flicks, water does not flow through the aesthetasc array (Mead and Koehl, 2000;Reidenbach et al, 2008;Koehl, 2011). Therefore, the sample of water that moves into the aesthetasc array during the downstroke is trapped between the aesthetascs during the return stroke and pause Mead, 2002;Koehl, 2006;Koehl, 2011), which last long enough for the odor molecules in the trapped water to diffuse to the surfaces of the aesthetascs (Stacey et al, 2002;Reidenbach et al, 2008).…”

“…During the slower return stroke and during the stationary pause between flicks, water does not flow through the aesthetasc array (Mead and Koehl, 2000;Reidenbach et al, 2008;Koehl, 2011). Therefore, the sample of water that moves into the aesthetasc array during the downstroke is trapped between the aesthetascs during the return stroke and pause Mead, 2002;Koehl, 2006;Koehl, 2011), which last long enough for the odor molecules in the trapped water to diffuse to the surfaces of the aesthetascs (Stacey et al, 2002;Reidenbach et al, 2008). The next downstroke replaces that water with a new sample; hence, each flick can be considered a 'sniff'.…”