Volumetric quantification of fluid flow reveals fish's use of hydrodynamic stealth to capture evasive prey

Abstract

In aquatic ecosystems, predation on zooplankton by fish provides a major pathway for the transfer of energy to higher trophic levels. Copepods are an abundant zooplankton group that sense hydromechanical disturbances produced by approaching predators and respond with rapid escapes. Despite this capability, fish capture copepods with high success. Previous studies have focused on the predatory strike to elucidate details of this interaction. However, these raptorial strikes and resulting suction are only effective at short range. Thus, small fish must closely approach highly sensitive prey without triggering an escape in order for a strike to be successful. We use a new method, high-speed, infrared, tomographic particle image velocimetry, to investigate three-dimensional fluid patterns around predator and prey during approaches. Our results show that at least one planktivorous fish (Danio rerio) can control the bow wave in front of the head during the approach and consumption of prey (copepod). This alters hydrodynamic profiles at the location of the copepod such that it is below the threshold required to elicit an escape response. We find this behaviour to be mediated by the generation of suction within the buccopharyngeal cavity, where the velocity into the mouth roughly matches the forward speed of the fish. These results provide insight into how animals modulate aspects of fluid motion around their bodies to overcome escape responses and enhance prey capture.

Keywords: animal–fluid interaction; hydrodynamic signals; predation; stealth predation; strain rate; tomography.

Figure 1.

Schematic diagram of experimental set-up, modified from [27]. (a) x–y view. (b) x–z view.

Figure 2.

Selected instance of the zebrafish Da. rerio performing a feeding strike on the copepod Di. leptopus. (a) Raw image from one of the four high-speed cameras. The location of the copepod is shown by a yellow oval for clarity. (b) The image from (a) with the visual hull mask applied to allow accurate fluid vector determination. Red spheres show the path of the escaping copepod before ingestion over t = 0–14 ms. (c) Simulated fish showing the locations of vertical planes I, II and III corresponding with the principal strain rate profiles in figure 2. Planes I and III are drawn at the edge of the fish's head, whereas plane II is drawn at the initial location of the copepod.

Figure 3.

Strain rate contours just prior to and during the initial phase of the feeding strike. Profiles are drawn at three locations across the head that correspond to planes I–III in figure 1. (a,b) Strain rates are reduced at plane II, which represents the location of the copepod. (c–e) As the strike begins strain rates increase sharply and extend further from the head as the copepod senses the disturbance and begins to mount an escape jump. Note that strong suction can also act to reduce the hydrodynamic disturbance of the rapid approach of the fish at the central plane in panel (e) II.

Figure 4.

Perpendicular planes at the opening of the mouth showing the spatial variation in principal strain rate. (a) Locations of planes shown in (b). Planes I and II transect the location of the copepod. (b) Raw image of the zebrafish approaching a copepod with two reconstructed views of the principal strain rate profiles which correspond to I and II in panel (a), and to the middle plane (II) in figure 2c.

Figure 5.

Comparison of representative strain rate profiles from: (a) normal (non-predatory swimming); (b) predatory approach to evasive prey represented in figure 2b II; and (c) approach to non-evasive prey. Scale bar, 1 mm.

Figure 6.

Mechanistic explanation for the presence of reduced strain rates during approaches to evasive prey. (a) Time series of the approach beginning when the fish approaches to within 5 mm of the copepod. (b) Result of tracking individual tracer particles at 2 ms intervals over the 100 ms approach duration represented in panel (a), confirming the presence of suction as the fish nears the copepod. Scale is millimetres per second.