How to surprise a copepod: Strike kinematics reduce hydrodynamic disturbance and increase stealth of suction-feeding fish

To capture prey with suction, fish must get sufficiently close to their prey to allow the suction flow to overwhelm the prey and draw it into the mouth. Both swimming towards the prey and suction flow create a hydrodynamic disturbance, which can elicit an escape response by the prey. Using particle image velocimetry, we measured flow speeds and derived fluid deformation rates at the location of the prey as bluegill sunfish fed. In front of the mouth, flows had a composite time-dependent nature. First, the bow wave pushed water away from the fish, but when the mouth opened and suction commenced, flow reversed and water deformation rates increased rapidly. Our inferences indicate that, at the prey, the approaching bluegill is detected primarily based on its suction-induced disturbance, rather than its bow wave–induced disturbance. A comparison of suction-induced disturbance with the signal produced by active suspension feeders indicated that fish are able to produce a more subtle disturbance than expected based on their flow speeds and mouth size alone. Jaw protrusion and the rapid opening of the mouth during the strike both help to minimize the signal available to the prey. We propose that the temporally quick strikes and high jaw protrusion that are seen in many zooplanktivorous teleosts represent adaptations that minimize the time available to prey for executing an escape response. In aquatic communities, predation on zooplankton by fish is a major trophic pathway (Kerfoot 1987; O’Brien 1987; Aksnes et al. 2004), and the nature of these predator– prey interactions is greatly influenced by the dense and viscous surrounding medium (Kiørboe et al. 1999; Visser 2001; Wainwright and Day 2007). Fish typically use suction feeding to capture zooplankton, and so they must get close enough to the prey so that the suction flows they generate can exert large enough hydrodynamic forces to pull the prey into their mouth (Holzman et al. 2007; Wainwright and Day 2007). However, aquatic predators push water as they move towards the prey, creating a hydrodynamic disturbance in front of them (Vogel 1994; Kiørboe et al. 1999; Visser 2001). Many aquatic organisms, including copepods, Cladocera, cephalopods, insect larvae, polychaetes, larvae and adult fishes, jellyfish, and other groups of aquatic metazoans can sense these hydrodynamic disturbances to detect predators (Fields and Yen 1997; reviewed by Visser 2001; Van Trump and McHenry 2008). Hydrodynamic disturbances are sensed when specialized sensory setae (e.g., in crustaceans, polychaetes) or sensory cells (fish, mollusks) respond to displacement, fluid velocity, or acceleration caused by the differential motion of the individual sensor and the body to which it is attached (Yen et al. 1992; Visser 2001; Van Trump and McHenry 2008). The relative motion of the sensors leads to nerve depolarization, which triggers the escape motor pattern. Following their approach to the prey, fish rapidly open their mouth to generate an external flow of water that pulls the prey into the mouth. Experimental evidence (FerryGraham et al. 2003; Day et al. 2005; Holzman et al. 2008a) and modeling studies (Muller et al. 1982; de Jong et al. 1987; Van Wassenbergh and Aerts 2009) reveal that these flows are exceptionally short-lived, lasting only 10–50 ms, and are restricted to an area very close to the mouth. Suction flows generate a region with strong spatial gradients in flow speed and high temporal instability. Although these steep gradients and extreme accelerations can potentially inform the prey of the attacking fish, the nature of these signals and how prey use them to avoid the striking fish is still unclear. Despite the pronounced reliance of fish on suction feeding to capture small prey, studies and modeling of fish–zooplankton interactions have attributed the hydrodynamic disturbance generated by fish predators to the bow wave produced by swimming (Viitasalo et al. 1998; Kiørboe and Visser 1999; Visser 2001). Previous research approaches to identify the hydrodynamic signals perceived by flow-sensing organisms used artificially generated fluid disturbances such as siphon flows (Fields and Yen 1997; Viitasalo et al. 1998; Kiørboe et al. 1999), moving and oscillating bodies (Buskey et al. 2002; Heuch et al. 2007), and flow chambers (Haury et al. 1980; Kiørboe et al. 1999; McHenry et al. in press). Although being instrumental in defining the sensory capabilities of small aquatic organisms, the signal produced by these artificial sources of hydrodynamic disturbances is likely an oversimplification of the highly dynamic hydrodynamic signal produced by suction-feeding fishes (Day et al. 2005). Moreover, from the perspective of the fish there may be a trade-off inherent in the effect of suction flows on the prey: fast flows will exert higher forces on the prey, but will also create a stronger disturbance that might lead to an earlier escape response. Our goal in this study was to characterize the hydrodynamic disturbance generated by the striking fish and ask whether and how fish attempt to reduce this disturbance. Specifically, we ask how rates of water deformation and flow (flow speed and strain rate) change in space and time during feeding strikes, and how the observed disturbance differs from that produced by other biological flow sources. * Corresponding author: [email protected] Limnol. Oceanogr., 54(6), 2009, 2201–2212 E 2009, by the American Society of Limnology and Oceanography, Inc.