Motion-driven flow in an unusual piscine nasal region
Introduction
Perception of smell in water requires transport of odorant molecules from the animal’s external environment to its olfactory epithelium. Because diffusion times in water are extremely long (Denny, 1993), aquatic animals must in the first instance rely on the bulk movement of water for odorant transport (Cox, 2008). The final stage of this process, however, involves diffusion alone (Vogel, 1994).
In fishes, four principal mechanisms may be used to generate bulk movement of water in the nasal region (‘olfactory flow’): (i) the beating of non-sensory cilia; (ii) the expansion and contraction of accessory sacs; (iii) respiration; and (iv) the movement of the fish relative to water (Cox, 2008). Mechanical agitation of the nasal region may also contribute to olfactory flow, but in a non-directional manner (Cox, 2008). Which mechanism(s) operate(s) depends on the species of fish.
Our aim here was to investigate olfactory flow in the adult garpike, Belone belone (Belonidae, Beloniformes, Teleostei). The garpike is a long, slender, marine fish with beak-like jaws (Fig. 1, Fig. 2) (Wheeler, 1969). Its elongated body, together with its prominent tail and the extreme posterior positioning of its dorsal and anal fins (Fig. 1), suggests that it is an active swimmer (Helfman et al., 2009). Indeed, according to Theisen et al. (1980, p. 169), adult garpike are known to swim ‘continuously and normally rather fast’.
The garpike has an unusual nasal region (Fig. 3). The olfactory epithelium of most non-beloniform fishes is enclosed in a nasal chamber, and is typically located on one or more thin folds, or lamellae (Hara, 1975, Zeiske et al., 1992, Cox, 2008). But in the garpike the olfactory epithelium is largely exposed to the external environment: it lines a triangular nasal cavity (Fig. 3B) and the surface of a papilla situated within the nasal cavity (Fig. 3B) (Blaue, 1884, Burne, 1909, Theisen et al., 1980, Cox, 2008). The nasal cavity widens caudally and its edges are sharp. There is a recess beneath the dorsal edge (Fig. 3C). The ventral apex may be somewhat elongated (Fig. 3B).
Olfactory flow in the garpike is likely to be generated primarily by its motion relative to water. Given that adult garpike are likely to be active swimmers, we assume that swimming is the main source of this motion, although an oncoming current could augment olfactory flow. Olfactory flow cannot be generated by the beating of non-sensory cilia, because the nasal region of the adult garpike lacks ciliated non-sensory cells (Theisen et al., 1980). Nor can it be generated by accessory sacs, as the garpike also lacks these anatomical devices. Some olfactory flow could be generated by respiration (the paired nasal regions are situated close to the mouth; Fig. 2), or mechanical agitation of the nasal region (e.g. by movement of the jaws). Mechanical agitation is likely to make only a minor contribution to olfactory flow given that other belonids typically swim with their jaws closed (B. Collette, personal communication).
In undertaking this study, we had two objectives. First, we wanted to demonstrate that olfactory flow in the garpike can be generated by swimming. Second, we wanted to determine how the unusual features of the garpike’s nasal region (nasal cavity, papilla, ventral apex) influence olfactory flow and the likely effect of these influences on odorant sampling in the garpike. As a subject for studying olfactory flow, the garpike was appealing for several, mainly practical, reasons. First, swimming could be simulated by flowing water over a static, life-like, plastic model of the garpike’s head. Moving fluid over a static model, a valid device that is also used to simulate flow over, for example, aircraft (Shapiro, 1961), is equivalent to moving the model through static water, but easier to achieve. Second, the garpike’s nasal region does not possess any moving parts that might complicate olfactory flow (e.g. the flexible lamellae typical of the nasal regions of other fishes). The rigidity of the nasal region could therefore be replicated in the plastic model. Third, the exposed nasal region allows direct observation of olfactory flow. Fourth, there is only one previous study of olfactory flow in the garpike, and this was mentioned only in passing (Zeiske and Hansen, 2005). That study found that the nasal papilla was ‘an adaptation to the hydrodynamic situation, including boundary layer effects of the longirostrate fish’, but no further details were given (Zeiske and Hansen, 2005, p. 22).
The present study forms part of a programme to understand the hydrodynamics of olfaction in fishes, an important but largely unexplored area (Cox, 2008, Abel et al., 2010, Holmes et al., 2011, Howard et al., 2013, Agbesi et al., 2016).
Section snippets
Specimens
Specimens were from the Natural History Museum, London, UK. The catalogue numbers and total lengths (Fig. 1, TL) of the 11 specimens of garpike (Belone belone) that we examined are BMNH 1939.6.27.3 (one specimen, TL = 61 cm), BMNH 1981.2.2.3–4 (two specimens, TL = 43 and 45 cm), BMNH 1995.8.22.5 (one specimen, TL = 42 cm), and BMNH 2005.4.27.24–30 (seven specimens, TL = 53–76 cm). All 11 specimens have well-preserved nasal regions (Fig. 3; cf. Theisen et al., 1980). Specimens BMNH 2005.4.27.24–30 comprise
Nasal morphology
Inspection of 11 garpike specimens with well-preserved nasal regions revealed variation in nasal morphology within the same specimen and between specimens (Fig. 3, which shows the nasal regions of six of these specimens). The papilla (Fig. 3B, dashed curve) was the most variable nasal feature, appearing in two principal forms that we refer to as type I and type II. Both types occurred with equal frequency. The type I papilla (e.g., Fig. 3A), situated in the centre of the nasal cavity, had a
Discussion
Our first objective was to show that olfactory flow in the garpike (i.e. bulk movement of water in its nasal region) can be generated by swimming. We achieved this (see Fig. 8 and Videos 1–12) by moving water over static, life-like, plastic models of the adult garpike’s head under physiologically relevant conditions (Reynolds numbers 700–2,000; angle of attack/yaw 0 ± 10°). Motion-driven olfactory flow occurred despite morphological variation in the garpike’s nasal region, variation that resulted
Conclusions
Olfactory flow in the adult garpike, Belone belone, can be generated by swimming, and occurs despite morphological variations in the nasal region. These variations can, however, influence the pattern of olfactory flow. Important influences on the pattern of olfactory flow are the position of the papilla in the nasal cavity and whether or not the papilla protrudes from the surface of the head. The inclination of a type I papilla may also affect the pattern of olfactory flow in the posterior
Acknowledgements
We thank Jim Askins for garpike specimen BMNH 2015.4.9.1, Joe Pender for the coordinates of where this specimen was caught, Laser Lines for 3D printing, Paul Frith for model assembly, Chen Chen, Joe Rodrigues, Mary Mahon, Ian Trussler, Simon Wharf, Jonathan White and Zhuoyi Ye for technical assistance, Harry Taylor and Kevin Webb for photography, Nina Martin for the X-ray image of BMNH 2015.4.9.1, Xavier Mear for German to English translation, Bruce Collette, Oliver Crimmen, Sherrie
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2020, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :Viscous entrainment of flow from the sturgeon's excurrent nostril may therefore be more effective than from the pike's (Vogel, 1978). Many of the limitations of the current study (and, where possible, their mitigation) are common to our previous studies (Abel et al., 2010; Agbesi et al., 2016a, 2016b; Garwood et al., 2019), and are discussed therein (see also Appendix A.3). One limitation of note in the current study was the lack of convexity in the eyes of the models of the juvenile pike (Fig. 3A).
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2019, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative PhysiologyCitation Excerpt :We addressed both questions by a) using dye to visualise olfactory flow in a plastic model of the sturgeon's head, and by b) simulating flow in a computational model of the sturgeon's head (computational fluid dynamics, CFD; Tu et al., 2018). For dye visualisation, the forward motion of the fish was simulated by flowing water over the static model in a flume (Agbesi et al., 2016b). We used both dye visualisation and CFD because the two techniques are complementary.
- 1
Present address: Department of Surgery and Cancer, Imperial College, London, W6 8RF, UK.
- 2
Present address: Henry Moseley X-ray Imaging Facility, University of Manchester, Manchester, M13 9PY, UK.