We have demonstrated that Mexican tetra fish can locate their depth with high fidelity by using hydrostatic pressure alone. Crucially, the fish can use hydrostatic pressure not only as a gradient, giving information about upward and downward movement but also as a distance-based cue that can allow precise localisation of their vertical position. This newly identified sensory capability indicates how fish can achieve the complex task of navigating through three-dimensional environments.
The basis of navigation in all animals, hinges on the individual knowing the spatial relationship between their current location and an intended destination. Although all animals inhabit a three-dimensional world, many, including humans, are constrained to travelling over surfaces with three degrees of freedom: two translational and one rotational14. The addition of the vertical dimension enlarges the size of the navigable space from a two-dimensional plane to a three-dimensional volume2, leading to a multiplicative increase in the complexity of a navigational task14,15,16. Reliable information on vertical position would therefore be a significant benefit for three-dimensional navigation.
Although it is likely that in the wild fish rely on multiple cues to navigate, a sense of pressure would be particularly useful when other cues are unavailable or unreliable, for example, in turbid waters where visual landmarks are absent or obscured, and in turbulent waters where olfactory plumes cannot provide fine-scale information. The stability and ubiquity of hydrostatic pressure in aquatic environments allow fish access to a reliable navigational cue and could explain why two separate experiments, each testing a different species, found that fish perceived vertical information as the more reliable cue when horizontal and vertical information conflicted.
The physiological mechanism underlying depth perception in fish is yet to be identified, although the swim-bladder has been implicated. In this putative mechanism, absolute depth is estimated during fast, steady vertical displacements by combining a measurement of vertical speed with a measurement of the fractional rate of change of swim-bladder volume. If this is the mechanism that these and other bony fish are using to sense their depth, there are likely to be important ecological and welfare consequences for fish that suffer barotrauma from angling or transit through hydroelectric power facilities, where the damage caused from exposure to rapid changes in barometric pressure may cause swim bladder ruptures17. Therefore, governments need to be aware of key migratory paths that fish use to move between feeding and breeding sites to enable them to protect important species. Similarly, fish that contract parasitic infections of the swim bladder are likely to find their vertical navigation is severely compromised. While there are currently no studies on the pressure sensing in fish with parasitic infections of the swim bladder, previous research has reported that infected Koi carp (Cyprinus carpio) are less able to achieve and sustain neutral buoyancy and demonstrate abnormal swimming behaviour18. Similarly, silver eels (Anguilla Anguilla) infected with a swim bladder nematode experienced a loss of buoyancy resulting in them expending more energy while swimming, impeding their migration19.
While the swim bladder appears to be a good candidate organ for sensing hydrostatic pressure in bony fish, many cartilaginous or deep-sea species do not possess a gas phase, despite still being able to navigate vertically. Previous research has suggested that instead of relying on fractional changes in swim bladder volume, these species may rely on the sensory afferents of their lateral line system; with evidence that swimming crabs (Callinectes ornatus), mud crabs (Panopeus herbstii) and dogfish (Scyliorhinus canicula) sense pressure changes via the bending of hair cells oriented to sense either vertical or horizontal displacements20. The ability of fish to use hydrostatic pressure to accurately locate a point in the vertical dimension may be important for fisheries management. Known points of interest, for example, food sites, refugia, heavily predated areas, present in the vertical column could be learned and remembered by fish, with them either returning to or avoiding these areas as necessary. Further field studies on individual fish and shoals of fish using hydrostatic pressure in this context are needed to identify how this cue is used both in the wild and in farmed fisheries.
Our findings reveal novel sensory information that A. mexicanus, and possibly other fish species, use to gain detailed navigational information over short distances in the vertical dimension. Extrapolating from this, we argue that it is likely that fish could use pressure to navigate over larger distances as the pressure magnitudes will increase as the vertical distance increases. Together, this study reveals a new sensory capacity that has great adaptive value in the fish’s volumetric world.
Source: Ecology - nature.com
