A novel mechanism for mechanosensory-based rheotaxis in larval zebrafish

Abstract

When flying or swimming, animals must adjust their own movement to compensate for displacements induced by the flow of the surrounding air or water1. These flow-induced displacements can most easily be detected as visual whole-field motion with respect to the animal’s frame of reference2. In spite of this, many aquatic animals consistently orient and swim against oncoming flows (a behavior known as rheotaxis) even in the absence of visual cues3,4. How animals achieve this task, and its underlying sensory basis, is still unknown. Here we show that in the absence of visual information, larval zebrafish (Danio rerio) perform rheotaxis by using flow velocity gradients as navigational cues. We present behavioral data that support a novel algorithm based on such local velocity gradients that fish use to efficiently avoid getting dragged by flowing water. Specifically, we show that fish use their mechanosensory lateral line to first sense the curl (or vorticity) of the local velocity vector field to detect the presence of flow and, second, measure its temporal change following swim bouts to deduce flow direction. These results reveal an elegant navigational strategy based on the sensing of flow velocity gradients and provide a comprehensive behavioral algorithm, also applicable for robotic design, that generalizes to a wide range of animal behaviors in moving fluids.

Whole-brain serial-section electron microscopy in larval zebrafish

“…Only one neuromast and its afferents lacked contralateral counterparts. This may be an important anatomical feature that facilitates comparisons of local velocity vector fields for detecting differential flow along the left and right sides, which is essential for larval zebrafish rheotaxis behaviour 28 .…”

Sensory ecology of the fish lateral‐line system: Morphological and physiological adaptations for the perception of hydrodynamic stimuli

“…Based on their behavioural data, Oteiza et al . () proposed a model, suggesting that fish use their mechanosensory lateral‐line system to first sense the local curl in the water ( i.e ., local rotations of the water) to detect the presence of flow and then to measure the temporal change of these curls after the swimming bouts to deduce flow direction.…”

“…Sutterlin and Waddy () suggested that the lateral‐line system serves as a detector of flow or pressure discontinuities, enabling the fish to maintain position with minimum expenditure of energy. This is in agreement with the mechanism proposed to underlie rheotaxis in A. mexicanus and D. rerio (Kulpa et al ., ; Oteiza et al ., ), However, whereas these two species rely on hydrodynamic information received by SNs, O. mykiss may rely mostly on information picked up by CNs. Sensing flow discontinuities with both lateral‐line subsystems is possible since the water motions behind an object contain discontinuities both in velocity and acceleration, which will be measured by SNs and CNs, respectively (Coombs et al ., ; Montgomery et al ., ).…”

“…A mechanism for mechanosensory-based rheotaxis based on local velocity gradients was proposed by Oteiza et al (2017). In this study, rheotaxis was investigated in larval D. rerio in the absence of any visual or other sensory information that could have potentially provided external references for the animals.…”

How fish feel the flow

“…But how does the lateral line sense local patterns of water motion, and how do fish use that information to navigate? On page 445, Oteiza et al 3 propose an elegant mechanism based on a robust principle of fluid dynamics, which only requires the fish to respond to the flow by making a simple choice between either continuing to swim without changing direction or making a turning manoeuvre.…”