Visually guided gradation of prey capture movements in larval zebrafish

Abstract

SUMMARYA mechanistic understanding of goal-directed behavior in vertebrates is hindered by the relative inaccessibility and size of their nervous systems. Here, we have studied the kinematics of prey capture behavior in a highly accessible vertebrate model organism, the transparent larval zebrafish (Danio rerio), to assess whether they use visual cues to systematically adjust their movements. We found that zebrafish larvae scale the speed and magnitude of turning movements according to the azimuth of one of their standard prey, paramecia. They also bias the direction of subsequent swimming movements based on prey azimuth and select forward or backward movements based on the prey's direction of travel. Once within striking distance, larvae generate either ram or suction capture behaviors depending on their distance from the prey. From our experimental estimations of ocular receptive fields, we ascertained that the ultimate decision to consume prey is likely a function of the progressive vergence of the eyes that places the target in a proximal binocular 'capture zone'. By repeating these experiments in the dark, we demonstrate that paramecia are only consumed if they contact the anterior extremities of larvae, which triggers ocular vergence and tail movements similar to close proximity captures in lit conditions. These observations confirm the importance of vision in the graded movements we observe leading up to capture of more distant prey in the light, and implicate somatosensation in captures in the absence of light. We discuss the implications of these findings for future work on the neural control of visually guided behavior in zebrafish. Supplementary material available online at

Finding and identifying simple objects underwater with active electrosense

“…Similar approaches have been studied in simulation for object identification by Ammari et al (2013Ammari et al ( , 2014 and Snyder et al (2012). Other common examples of movement for sensory acquisition include eye movements and movement of the sonar probe in echolocating bats (Land, 1999;Yovel et al, 2010;Patterson et al, 2013). For example, when identifying object geometry using vision, animals move closer and foveate.…”

Zebrafish learn to forage in the dark

“…Foraging is characterized by spontaneous intermittent swimming that is interrupted by targeted movement toward prey upon detection (Fuiman and Webb, 1988;Budick and O'Malley, 2000). This targeted swimming includes a series of pectoral fin and tail motions that serve to align the rostrum with the prey (McElligott and O'Malley, 2005;Patterson et al, 2013). Once in a close position (<0.5 mm), the larva attempts to capture the prey with a suction-feeding strike (Patterson et al, 2013).…”

“…This targeted swimming includes a series of pectoral fin and tail motions that serve to align the rostrum with the prey (McElligott and O'Malley, 2005;Patterson et al, 2013). Once in a close position (<0.5 mm), the larva attempts to capture the prey with a suction-feeding strike (Patterson et al, 2013).…”

“…Under illumination, larvae respond to zooplankton at a greater distance (<3 mm) than in the dark (<1 mm) (Gahtan et al, 2005;Bianco et al, 2011;Patterson et al, 2013). Larvae strike at prey in the dark with a relatively low frequency and each strike is less successful than when they can see (Westphal and O'Malley, 2013).…”

“…These morphological changes alter the frequency response of the neuromasts such that they become sensitive to pressure gradients in the flow field (van Netten, 2006). These changes are likely to be important to foraging because larval fish appear to be responsive to prey motion around the head (Bianco et al, 2011;Patterson et al, 2013). The present study included a morphological analysis of the superficial neuromasts during larval growth to test whether changes in morphology might account for the improvement of foraging in the dark with age.…”