Olfactory flow in the sea catfish, Ariopsis felis (L.): Origin, regulation, and resampling.

The olfactory epithelium of the sea catfish, Ariopsis felis, is found on a pinnate array of lamellae (the olfactory rosette) housed within a nasal chamber. The nasal anatomy of A. felis suggests an ability to capture external water currents. We prepared models from X-ray micro-computed tomography scans of two preserved specimens of A. felis. We then used dye visualisation and computational fluid dynamics to show that an external current induced a flow of water through a) the nasal chamber and b) the sensory channels of the olfactory rosette. The factors responsible for inducing flow through the nasal chamber are common to fishes from two other orders. The dye visualisation experiments, together with observations of sea catfishes in vivo, indicate that flow through the nasal chamber is regulated by a mobile nasal flap. The position of the nasal flap - elevated (significant flow) or depressed (reduced flow) - is controlled by the sea catfish's movements. Flow in the sensory channels of the olfactory rosette can pass through either a single channel or, via multiple pathways, up to four consecutive channels. Flow through consecutive sensory channels (olfactory resampling) is more extensive at lower Reynolds numbers (200 and 300, equivalent to swimming speeds of 0.5-1.0 total lengths s-1), coinciding with the mean swimming speed of the sea catfishes observed in vivo (0.6 total lengths s-1). Olfactory resampling may also occur, via a vortex, within single sensory channels. In conclusion, olfactory flow in the sea catfish is regulated and thoroughly sampled by novel mechanisms.

The functional nasal anatomy of the pike, Esox lucius L.

Olfactory flow in fishes is a little-explored area of fundamental and applied importance. We investigated olfactory flow in the pike, Esox lucius, because it has an apparently simple and rigid nasal region. We characterised olfactory flow by dye visualisation and computational fluid dynamics, using models derived from X-ray micro-computed tomography scans of two preserved specimens. An external current induced a flow of water through the nasal chamber at physiologically relevant Reynolds numbers (200-300). We attribute this externally-induced flow to: the location of the incurrent nostril in a region of high static pressure; the nasal bridge deflecting external flow into the nasal chamber; an excurrent nostril normal to external flow; and viscous entrainment. A vortex in the incurrent nostril may be instrumental in viscous entrainment. Flow was dispersed over the olfactory sensory surface when it impacted on the floor of the nasal chamber. Dispersal may be assisted by: the radial array of nasal folds; a complementary interaction between a posterior nasal fold and the ventral surface of the nasal bridge; and the incurrent vortex. The boundary layer could delay considerably (up to ~ 3 s) odorant transport from the external environment to the nasal region. The drag incurred by olfactory flow was almost the same as the drag incurred by models in which the nasal region had been replaced by a smooth surface. The boundary layer does not detach from the nasal region. We conclude that the nasal bridge and the incurrent vortex are pivotal to olfaction in the pike.

Olfactory flow in the sturgeon is externally driven.

Fluid dynamics plays an important part in olfaction. Using the complementary techniques of dye visualisation and computational fluid dynamics (CFD), we investigated the hydrodynamics of the nasal region of the sturgeon Huso dauricus. H. dauricus offers several experimental advantages, including a well-developed, well-supported, radial array (rosette) of visible-by-eye olfactory sensory channels. We represented these features in an anatomically accurate rigid model derived from an X-ray scan of the head of a preserved museum specimen. We validated the results from the CFD simulation by comparing them with data from the dye visualisation experiments. We found that flow through both the nasal chamber and, crucially, the sensory channels could be induced by an external flow (caused by swimming in vivo) at a physiologically relevant Reynolds number. Flow through the nasal chamber arises from the anatomical arrangement of the incurrent and excurrent nostrils, and is assisted by the broad, cartilage-supported, inner wall of the incurrent nostril. Flow through the sensory channels arises when relatively high speed flow passing through the incurrent nostril encounters the circular central support of the olfactory rosette, decelerates, and is dispersed amongst the sensory channels. Vortices within the olfactory flow may assist odorant transport to the sensory surfaces. We conclude that swimming alone is sufficient to drive olfactory flow in H. dauricus, and consider the implications of our results for the three other extant genera of sturgeons (Acipenser, Pseudoscaphirhynchus and Scaphirhynchus), and for other fishes with olfactory rosettes.

Motion-driven flow in an unusual piscine nasal region.

Fishes have several means of moving water to effect odorant transport to their olfactory epithelium ('olfactory flow'). Here we show that olfactory flow in the adult garpike Belone belone (Belonidae, Teleostei), a fish with an unusual nasal region, can be generated by its motion relative to water (swimming, or an external current, or both). We also show how the unusual features of the garpike's nasal region influence olfactory flow. These features comprise a triangular nasal cavity in which the olfactory epithelium is exposed to the external environment, a papilla situated within the nasal cavity, and an elongated ventral apex. To perform our investigation we first generated life-like plastic models of garpike heads from X-ray scans of preserved specimens. We then suspended these models in a flume and flowed water over them to simulate swimming. By directing filaments of dye at the static models, we were able to visualise flow in the nasal regions at physiologically relevant Reynolds numbers (700-2,000). We found that flow of water over the heads did cause circulation in the nasal cavity. Vortices may assist in this circulation. The pattern of olfactory flow was influenced by morphological variations and the asymmetry of the nasal region. The unusual features of the nasal region may improve odorant sampling in the garpike, by dispersing flow over the olfactory epithelium and by creating favourable conditions for odorant transport (e.g. steep velocity gradients). Unexpectedly, we found that the mouth and the base of the garpike's jaws may assist the sampling process. Thus, despite its apparent simplicity, the garpike's nasal region is likely to act as an effective trap for odorant molecules.

Complex flow in the nasal region of guitarfishes.

Scent detection in an aquatic environment is dependent on the movement of water. We set out to determine the mechanisms for moving water through the olfactory organ of guitarfishes (Rhinobatidae, Chondrichthyes) with open nasal cavities. We found at least two. In the first mechanism, which we identified by observing dye movement in the nasal region of a life-sized physical model of the head of Rhinobatos lentiginosus mounted in a flume, olfactory flow is generated by the guitarfish's motion relative to water, e.g. when it swims. We suggest that the pressure difference responsible for motion-driven olfactory flow is caused by the guitarfish's nasal flaps, which create a region of high pressure at the incurrent nostril, and a region of low pressure in and behind the nasal cavity. Vortical structures in the nasal region associated with motion-driven flow may encourage passage of water through the nasal cavity and its sensory channels, and may also reduce the cost of swimming. The arrangement of vortical structures is reminiscent of aircraft wing vortices. In the second mechanism, which we identified by observing dye movement in the nasal regions of living specimens of Glaucostegus typus, the guitarfish's respiratory pump draws flow through the olfactory organ in a rhythmic (0.5-2 Hz), but continuous, fashion. Consequently, the respiratory pump will maintain olfactory flow whether the guitarfish is swimming or at rest. Based on our results, we propose a model for olfactory flow in guitarfishes with open nasal cavities, and suggest other neoselachians which this model might apply to.

Functional nasal morphology of chimaerid fishes.

Holocephalans (chimaeras) are a group of marine fishes comprising three families: the Callorhinchidae (callorhinchid fishes), the Rhinochimaeridae (rhinochimaerid fishes) and the Chimaeridae (chimaerid fishes). We have used X-ray microcomputed tomography and magnetic resonance imaging to characterise in detail the nasal anatomy of three species of chimaerid fishes: Chimaera monstrosa, C. phantasma and Hydrolagus colliei. We have shown that the nasal chamber of these three species is linked to the external environment by an incurrent channel and to the oral cavity by an excurrent channel via an oral groove. A protrusion of variable morphology is present on the medial wall of the incurrent channel in all three species, but is absent in members of the two other holocephalan families that we inspected. A third nasal channel, the lateral channel, functionally connects the incurrent nostril to the oral cavity, by-passing the nasal chamber. From anatomical reconstructions, we have proposed a model for the circulation of water, and therefore the transport of odorant, in the chimaerid nasal region. In this model, water could flow through the nasal region via the nasal chamber or the lateral channel. In either case, the direction of flow could be reversed. Circulation through the entire nasal region is likely to be driven primarily by the respiratory pump. We have identified several anatomical features that may segregate, distribute, facilitate and regulate flow in the nasal region and have considered the consequences of flow reversal. The non-sensory cilia lining the olfactory sensory channels appear to be mucus-propelling, suggesting that these cilia have a common protective role in cartilaginous fishes (sharks, rays and chimaeras). The nasal region of chimaerid fishes shows at least two adaptations to a benthic lifestyle, and suggests good olfactory sensitivity, with secondary folding enhancing the hypothetical flat sensory surface area by up to 70%.

Functional morphology of the nasal region of a hammerhead shark.

We describe several novel morphological features in the nasal region of the hammerhead shark Sphyrna tudes. Unlike the open, rounded incurrent nostril of non-hammerhead shark species, the incurrent nostril of S. tudes is a thin keyhole-like aperture. We discovered a groove running anterior and parallel to the incurrent nostril. This groove, dubbed the minor nasal groove to distinguish it from the larger, previously described, (major) nasal groove, is common to all eight hammerhead species. Using life-sized plastic models generated at 200 microm resolution from an X-ray scan, we also investigated flow in the nasal region. Even modest oncoming flow speeds stimulate extensive, but not complete, circulation within the model olfactory chamber, with flow passing through the two main olfactory channels. Flow crossed from one channel to another via a gap in the olfactory array, sometimes guided by the interlamellar channels. Major and minor nasal grooves, as well as directing flow into the olfactory chamber, can, in conjunction with the nasal bridge separating incurrent and excurrent nostrils, limit flow passing into the olfactory chamber, possibly to protect the delicate nasal structures. This is the first simulation of internal flow within the olfactory chamber of a shark.