While few data are available for later life stages, the kinematics of early-larval zebrafish preying upon Paramecium multinucleatum have been described in some detail. Predation on these small, 200–300 μm long prey items was described using high-speed imaging. Prey tracking, at this stage, consists of a variable number and combination of orienting turns and forward swims that serve to better align the fish to its prey by decreasing its angular deviation and distance (McElligott and O'Malley, 2005; McClenahan et al., 2012; Patterson et al., 2013). The orienting turns are kinematically distinct from previously described larval turns (routine and escape) and were called “J-turns” because of their rhythmic J-bends that are unilateral, far caudal (85.5% body length) and of high amplitude (bend angles >90°). The forward swim bouts observed during tracking are indistinguishable from previously described slow swims (Budick and O'Malley, 2000). These slow swims involve rhythmic tail beats that propel the fish forward, closer to the prey. In addition, there are a variety of fin movements associated with swimming and predatory behaviors (Thorsen et al., 2004; Danos and Lauder, 2007; McClenahan et al., 2012).

The consummatory phase of larval feeding, termed a capture swim, consists of a distinctive maneuver in which “fine axial motor control” generates rapid, precise acceleration through the prey item's location (Borla et al., 2002). The capture swim is initiated only when the larva is within a 3–7° heading of the Paramecium and is associated with a peak in the instantaneous tail beat frequency and velocity, and concomitant propulsion of the fish forward to capture the Paramecium. It appears to be facilitated by vergence eye movements (Bianco et al., 2011; Patterson et al., 2013). Peak velocity during this capture event is around 30 μm/ms compared to the ubiquitous “slow swims,” which have comparably slower linear velocities of about 15 μm/ms. Predation by larvae thus consists of a series of discrete locomotor maneuvers and is innate in that successful strikes are seen from the first feeding episodes. For juveniles and adults, there are so far only preliminary reports about prey tracking and strike kinematics (Bonaiuto et al., 2007; Westphal and O'Malley, 2010).

In regards to sensory mechanisms of predation, there is accumulating data specifically for larval sensory controls. Larval zebrafish are known to dramatically reduce prey consumption when placed in the dark and do not appear to exhibit the distinct tracking and capture maneuvers used in the light (McElligott and O'Malley, 2005). However, the precise relationship between visual signals and the distinct motor elements of larval prey tracking and capture remain undefined. Gahtan et al. (2005) investigated the role of the optic tectum, (homologous to the mammalian superior colliculus) in the guidance of zebrafish feeding episodes. Bilateral tectal ablations were shown to decrease, but not eliminate, feeding in larval zebrafish (also see Burrill and Easter, 1994, regarding other retinorecipient areas). Lakritz mutants, which lack retinal ganglion cells, also show a deficit in feeding rate (Gahtan et al., 2005). More recent data has defined key criteria of the visual stimulus (Bianco et al., 2011; Patterson et al., 2013) and suggested a role for binocular visual information. These data notwithstanding, feeding is not abolished in the dark and other sensory modalities may contribute.

The mechanosensory lateral line (Münz, 1989) is a plausible candidate for guiding zebrafish prey capture in the dark, and might also provide short range sensory information to aid predation in circumstances where visual information is readily available. The lateral line is found in fishes and aquatic amphibians and contributes to a variety of behaviors including rheotaxis (Montgomery et al., 1997), eddy chemotaxis (Gardiner and Atema, 2007), station holding (Montgomery et al., 2003), hydrodynamic imaging (Hassan, 1989; Windsor et al., 2008) and predator avoidance (McHenry et al., 2009; Stewart et al., 2013). Of note here is the possible role for lateral line in prey capture (New et al., 2001; Pohlmann et al., 2004), that may derive from its specialized structures. The posterior lateral line consists of an array of neuromasts running along the lateral surfaces of the fish's trunk. This is complemented by an anterior lateral line system comprised of clusters of neuromasts located around the head region.

The further specialization of the lateral line into canal and superficial systems of neuromasts might also facilitate prey detection and tracking. Superficial neuromasts contribute to the detection of water currents moving over the surface of the fish and facilitate the rheotaxic behavioral response (Montgomery et al., 1997; Olszewski et al., 2012). The amplitude of cupula displacement is proportional to the velocity of water flow which enables water velocity to be encoded by the afferent firing rate (Münz, 1989). In contrast, canal neuromasts are located in ossified canals between two pores. When there is a pressure difference at the surface, water flows through the pores, deflecting the neuromast. The canal neuromasts are likely responsible for detection of water vibrations created by a predator (McHenry et al., 2009) or prey item (Montgomery, 1989; Janssen and Corcoran, 1993; Montgomery et al., 2002, 2003; Pohlmann et al., 2004; Bassett et al., 2007). The lateral line (perhaps the anterior neuromasts) was suggested as a possible releaser of the capture swim, but at present there are only preliminary reports on the contribution of lateral line to predation by larval and juvenile zebrafish (Bonaiuto et al., 2007; Westphal and O'Malley, 2010).

To better understand the ontogeny and neural control of zebrafish predation, more information is needed about the changing kinematics and strategy of predation, as well as the sensory controls that enable this critical behavior. Using high-speed behavioral imaging, we document a rapid increase in the sophistication and efficacy of predatory episodes that is highlighted by (1) a fusion of basic motor maneuvers into seamless “homing strikes” and (2) a surprisingly flexible array of motor patterns (including bend sequences) that allows juvenile fish to effectively strike throughout much of the imaging arena. In addition, we provide evidence that the lateral line system contributes to predatory success across ontogenetic stages.

Videos were viewed frame-by-frame using NIH Image J. The following measurements and calculations were made.

Paramecia and Artemia were filmed at 250 frames per second for 4 s. Subsequently, videos were analyzed using Image J to determine velocity. Distance traveled between successive frames was divided by the time elapsed to generate instantaneous velocities (μm/ms). The peak instantaneous velocities recorded from 5 individuals were averaged to determine the peak velocity for each species. Average instantaneous velocities were also determined for each individual and averaged over 5 individuals to determine the average velocity for each species.

In the example juvenile feeding episode shown (Figure 3C), the juvenile moves continuously from episode initiation through to striking the Artemia. Absent pauses, the total elapsed times of juvenile feeding episodes can be much smaller (note the different time scales in Figures 3A–C). Also, the example of Figure 3C has no substantive “forward swimming” component or rhythmic trunk bending. Instead, after a caudal kink in the trunk at 20 ms, there is a pronounced bend to the right that helps propel the juvenile through the Artemia's location. This is but one example and juvenile strike patterns are quite varied as described below.

Replay of high-speed video of prey capture episodes allowed them to be classified as single maneuver, or multi-maneuver (using discrete movement bouts separated by pauses). For instance, a 5-day-old larval episode might consist of: J-turn – pause – slow swim – pause – capture swim. As zebrafish mature, the discrete tracking and strike maneuvers used by early larvae disappear. Most juvenile and all adult zebrafish instead display a single, continuous (and often complex) feeding maneuver where orientation and approach to a prey item are merged together. Because these fluid maneuvers often cover significant distance and/or show substantial direction change, they are referred to here as “homing strikes.” In quantitative terms, all early larval feeding episodes (n = 43) contain multiple movement bouts, while 73% of late larval feeding episodes (n = 37) used two or more maneuvers and only 24% of juvenile episodes (n = 34) were multi-maneuver. Thus, the large majority of juvenile and all adult locomotor-driven feeding episodes (n = 38) were single maneuver episodes, i.e., homing strikes.

Relative swim velocity is important in that faster velocities may enable capture of faster prey. Figure 4 summarizes mean peak velocity (in μm/ms) of the main prey items studied here, Paramecia and Artemia, along with the zebrafish mean peak velocities which, at all stages, are higher than the prey items consumed during those stages. Early larvae show peak velocities ranging from 22 to 79 μm/ms, much faster than Paramecia which swim at an average velocity of 0.61 ± 0.1 μm/ms s.d., and a peak velocity of 1.72 ± 0.3 μm/ms, s.d. Artemia swim at an average velocity of 5.19 ± 0.7 μm/ms s.d., and a peak velocity of 17.6 ± 2.3 μm/ms, s.d. Artemia are preyed upon by late larval and juvenile zebrafish, which have peak velocities ranging from 21 to 89 μm/ms and 32 to 94 μm/ms, respectively. Zebrafish can thus attain peak velocities that are much faster than these laboratory prey items.

The total duration of individual feeding episodes (which includes tracking and capture components) decreases over ontogeny (Figure 5A). Early larval feeding episodes are the longest, and duration falls dramatically by the juvenile and adult stages. The early and late larval episodes were significantly longer than juvenile and adult feeding episodes (p < 0.005), demonstrating that older fish are able to capture prey items more quickly (at least within the constraints of our feeding arena). Also calculated was cumulative pause time for all episodes that included multiple maneuvers (n = 82). This fell sharply with development (Figure 5B). The early larval cumulative pause durations (mean = 534 ± 402 ms, s.d.), were much longer than those of both late larval (326 ± 329 ms, s.d.) and juvenile (115 ± 146 ms, s.d.) fish. Because adults were never observed to pause during individual feeding episodes, they are not represented in Figure 5B.

In terms of swimming speed, both peak strike velocity and episode velocity (average speed across an entire episode) were measured. Normalized episode velocity, which includes any pause time, increased over ontogeny (n = 157, Figure 6A), primarily in the late larval to juvenile transition. The data points for early larvae (4 to 6 mm TL) are fairly clustered, in contrast to the broader distributions for older fish. A subset of feeding episodes (n = 40), of sufficient quality for automated analysis, was further analyzed to determine the normalized peak velocity and peak tail beat frequency for feeding strikes. An exponential decrease in normalized peak velocity (BL/s) is seen as fish mature (Figure 6B). Concurrently, there is a sharp decline in peak tail beat frequency (measured in Hz; Figure 6C), indicating a change in the operation of neural oscillators in spinal cord.

When measured in absolute terms (μm/ms), early larvae were (somewhat unexpectedly) seen to exhibit absolute peak swimming velocities roughly comparable to those of juvenile and even adult zebrafish (Figure 7), although adults showed the highest recorded velocities. In contrast, the overall episode velocity increased dramatically, especially across the larval to juvenile transition. These results are explained by the pronounced but brief burst of acceleration seen in early larval capture swims which yield high peak velocities, whereas episode velocities are low due to the frequent pauses. The differences between episode vs. peak velocity are statistically significant for both early and late larvae (p < 0.0005).

The angles and distances from which feeding episodes are launched are another measure of predatory capability. Figure 8A shows the offset angles from which both episodes (E) and final strikes (S) are launched (n = 157). Offset is the angle between the zebrafish's orientation and the direction to the prey item, so that a 90° offset angle would require a net right or left turn to approach the prey. The strike offset angle is miniscule for early larvae, but increases markedly across development. In contrast, episode offset angles begin large and increase further. For both early and late larvae, the offset angles are significantly smaller for strikes than episodes (p < 0.005). By the adult stage, all feeding episodes are comprised of single movement bouts and so the episode and strike offset angles are essentially the same and represent an ability to strike throughout much of the feeding arena. As the box plots indicate, zebrafish of all ages tend to initiate predatory episodes within ±60° of their heading. In regards to strike distance, Figure 8B shows that strikes (S) are launched from very close distances in early larvae, but this rises many fold in juveniles and adults, even as normalized to body length. Feeding episodes (E), however, are launched at similar (normalized) distances across age groups.

Figure 9 illustrates the diversity of strike patterns used by juvenile zebrafish. These early data were collected in a smaller, relatively confined feeding arena that may have imposed greater demands in terms of striking at prey items. The three exemplar strikes all consist of a single bout of continuous trunk movement, with precise orienting turns and propulsion executed in close coordination with jaw protrusions (arrows), hence the term “homing strikes.” The first example (Figure 9A) consists of a single large but slow bend that precisely orients the juvenile towards the Artemia (inside circle). There are no subsequent bends, so this strike lacks the rhythmic component of escape and slow swimming behaviors. In contrast, the homing strike in Figure 9B consists of an initial turn followed by five cycles of slow swimming, after which the larva coasts directly through the Artemia's location.

The last example (Figure 9C) documents more flexible regulation of axial musculature. This homing strike consists of three bends in total beginning with a large, sustained and rostral bend (turn) that orients the rostral trunk towards the Artemia. Two smaller, caudal bends are superimposed upon the rostral bend and seem to propel the well-oriented rostral trunk directly towards the Artemia. This particular strategy seems related to the close proximity of the Artemia which could be seen swimming near the right eye of the juvenile, eventually reaching a suitable position for a strike to be launched (black circles indicate Artemia's location at different times). Jaw protrusions and Artemia are more readily observed when viewing movies, versus still photos, but the jaw protrusion (arrow) in the last frame of Figure 9C is evident and emerges at the proper time for efficient prey capture. The kinematic features of these exemplar homing strikes differ sufficiently from one another as to be considered distinct predatory strategies.

In some first feeding episodes, young larvae oriented and moved towards a nearby prey item, but did not consume it. Failed episodes resulted from both misses and, more frequently, aborted episodes, where items were tracked and approached, but no strike was launched. In comparing successful and aborted episodes (Figure 10), both showed larvae orienting via J-turns towards a Paramecium and approaching it, but in the aborted case (lower row), the larva abruptly turned away terminating the feeding episode. Table 1 provides a comparison of 19 successful and 19 aborted feeding episodes.

The decision of early larval fish to abort a feeding episode did not correlate with either prey velocity or distance to prey at strike initiation/abort (in the aborted trials, the prey were slightly closer). Aborted efforts had only modestly longer episode durations, but the final pause duration, after which the larva either strikes at the Paramecia or turns away, showed a large difference: the final pause of aborted episodes was 8-fold longer than those seen in successful episodes. The cause of aborted episodes is unknown, but may have to do with the sensory detection of prey items, as considered next.

While zebrafish are primarily visual predators, they do feed in the dark, albeit at lower rates. Using infrared (IR) illumination, zebrafish and prey movements were recorded in the dark. A representative episode is shown in the montages in Figure 11, where an Artemia (inside white circle) can be seen swimming alongside a juvenile for about 800 ms (Figure 11A). Then, the zebrafish abruptly turns and makes several attempts to capture the Artemia, beginning about the second frame in Figure 11B (pectoral fin movements are indicated by arrows). Two unsuccessful strikes (indicated by jaw protrusions, asterisks) occur at 856 and 900 ms, while a third strike at 968 ms was successful.

The mechanosensory lateral line is a candidate system for mediating prey capture in the dark. To investigate this possibility, feeding rates of late larval (n = 96) and juvenile (n = 68) zebrafish (that had not been fed for 24 h) were measured under four different sensory conditions: (a) Light with lateral line intact; (b) Light with lateral line lesioned (by neomycin exposure); (c) Dark with lateral line intact; (d) Dark with lateral line lesioned. After housing fish with 30 Artemia for 2 h, the remaining Artemia were counted (Table 2). Both late larvae and juveniles consumed far more Artemia in the light, as compared to dark. In the “Light + Neomycin” group, feeding rates were not significantly depressed, but the combination of “Dark + Neomycin” leads to dramatically lower feeding rates, with larvae consuming about 37-fold fewer Artemia than during normal feeding in the light.

To further investigate the impact of lateral line lesioning, high-speed recordings were made of normal and neomycin-treated fish. The average value of feeding success (given as the percentage of successful strikes) was lower for all age groups after neomycin exposure (Figure 12A). The drop in feeding success in the late larval, 24 dpf group was statistically significant (p < 0.05). The median success rate of early (8 dpf) larvae also dropped, from 50% to about 10%, and while this result was not statistically significant, some of these larvae captured zero Artemia. Early larvae have a more difficult time with Artemia (vs. Paramecia) because of their size, but the drop-off in success rate with neomycin suggests a role for lateral line in guiding the capture swim, which is potentially mediated by anterior neuromasts, shown stained with DASPEI in Figure 12B. The adult fish were most successful with many adults showing 100% success in both the control and neomycin groups.

Strike distances and success rates were compared in light vs. dark conditions, as shown for feeding episodes of nine 39-dpf juvenile zebrafish recorded under IR vs. normal illumination (Figure 13A). Of nine feeding events recorded in the dark, five were successful (55%), compared with 9/10 (90%) successful feeding episodes from the same fish in the light. During dark feeding episodes, juveniles initiated feeding at 1.55 ± 1.11 mm from the prey, but launched strikes from 4.29 ± 1.96 mm in the light (p-value = 0.02) (Figure 13B). This fits with the longer range of vision vs. lateral line, which functions better at short distances. While sustained tracking movements were not apparent in the dark, in agreement with data of Patterson et al. (2013) on larvae, our modest set of recorded dark feeds precludes strong conclusions on juveniles.

The predatory capabilities of early larval zebrafish are limited but presumably sufficient for natural prey items, although ecological details remain sparse (Engeszer et al., 2007a,b; Spence et al., 2007, 2008). Over the next 4 weeks, motor performance improves rapidly and is highlighted by the fusion of discrete early larval maneuvers into seamless homing strikes. This is not a simple “merger” of tracking and capture movements because J-turns and the kinematic features of capture swims disappear. Instead, what emerges is an ability to fuse orientation and propulsion, which allows juveniles to strike prey items over a wide range of angles and distances within the arena (Figure 8). This fusion of tracking and capture maneuvers also enables a sharp drop in feeding episode duration (Figure 5), while the episode velocity increases in both normalized and absolute terms (Figures 6, 7). In contrast, early larvae are able to launch their final strike only when they are very close and precisely aligned with the prey (Figure 8), although feeding episodes are initiated from much larger directions and distances.

This is not to discount early larval efforts, which are quite successful from first feedings, but rather reflects changing capabilities as zebrafish grow in size and begin to strike larger and faster prey items. The observed peak feeding velocities of larval and juvenile zebrafish do not change greatly across ontogeny, in absolute terms (Figure 7), although they exceed the velocity of our laboratory prey items, Paramecia and Artemia (Figure 4). What seems more important are the shorter overall durations of episodes: faster relative velocities may often be useful in predation, but a more rapid rate of capture should be advantageous in terms of total acquired nutrition and in terms of competition with conspecifics, if resources are limited.

Many fishes visually hunt prey items (Drost, 1987; Batty et al., 1990; Job and Bellwood, 1996; New et al., 2001; Rice and Westneat, 2005; Fleisch and Neuhauss, 2006) and vision is central to larval zebrafish feeding, based on the role of optic tectum (Gahtan et al., 2005), the lack of tracking movements in the dark (McElligott and O'Malley, 2005; Patterson et al., 2013) and the elicitation of J-turns by artificial visual stimuli (Bianco et al., 2011). Vision remains the predominant sensory modality in older larvae and juveniles, given the large drop in feeding rates seen in the dark (Table 2) and the longer strike distance and better accuracy in light vs. dark conditions (Figure 13). Feeding continues, however, at a low rate in darkness and juveniles can execute targeted predatory maneuvers (Figure 11), suggesting use of another modality for prey detection.

Lateral line contributes to predation in a variety of fishes (Montgomery, 1989; New et al., 2001; Pohlmann et al., 2004). Table 2 shows that ablation of lateral line sensors with neomycin decreases feeding rate in both late larvae and juveniles, but not to nearly the extent as darkness. Neomycin also decreases strike accuracy in the light, in both early and late larvae (Figure 12), but older juveniles fare better, perhaps because visual targeting and/or inertia of the strikes makes the lateral line less necessary. The combination of darkness and neomycin has the most profound effect, reducing feeding to very low levels in late larvae and juveniles (Table 2). Early larvae strike (initiate capture swims) from very close range (Figure 8B), and anterior neuromasts (visualized in Figure 12) may aid this behavior (New et al., 2001; Pohlmann et al., 2004). Our neomycin data, however, are not definitive regarding capture swim modality because these swims remain well formed in the Light + Neomycin condition. Contributions to the control of capture swims by olfactory and gustatory senses (Caprio, 1978; Kanwal and Finger, 1997; Friedrich et al., 2004; Gardiner and Atema, 2007) or tactile interactions (Patterson et al., 2013) remain a possibility.

Optic tectum is the largest visual structure in the teleost brain (Burrill and Easter, 1994; Wullimann et al., 1996), and accumulating evidence suggests a role in zebrafish prey capture (Gahtan et al., 2005; Del Bene et al., 2010; Bianco et al., 2011). The larval optic tectum already has a diversity of cell types (Niell and Smith, 2005; Sumbre et al., 2008; Gabriel et al., 2012) which is potentially greater by the juvenile stage and might contribute to the visual analyses that guide homing strikes. Tectum appears to play a central role in sensorimotor transformations that convert spatial information into motor commands (Ewert, 1987; Scott and Baier, 2009; Ahrens et al., 2012; Grama and Engert, 2012), presumably in conjunction with brainstem circuits and associated descending pathways that include the reticulospinal array and nMLF (Lee and Eaton, 1991; Foreman and Eaton, 1993; O'Malley et al., 1996; Zelenin et al., 2001; Bosch and Roberts, 2001; Gahtan et al., 2002; Gahtan and O'Malley, 2003; Sankrithi and O'Malley, 2010). Details of these transformations are just beginning to be understood (Del Bene et al., 2010; Bianco et al., 2011; Koyama et al., 2011; Fajardo et al., 2013).

Larval J-turns require neural controls distinct from other larval turns being (1) of much slower angular velocity than escape turns (Eaton et al., 1991; Liu and Fetcho, 1999) and (2) kinematically distinct from spontaneous routine turns (Budick and O'Malley, 2000; Danos and Lauder, 2007) which are also used in optomotor behaviors (Roeser and Baier, 2003; Day et al., 2006; Burgess and Granato, 2007; Orger et al., 2008). J-turns are incremental “turn left” or “turn right” responses (Bianco et al., 2011) that achieve precise orientation in a stepwise fashion. The significant pauses between discrete tracking maneuvers (Figures 3, 5) might allow for visual updating of direction and distance, after which the correct next maneuver can be selected. Recent optogenetic results suggest there are specialized tectal circuits for J-turns and that a winner-take-all mechanism enables a specific behavior (J-turn vs. slow swim) to be selected (Fajardo et al., 2013). While early larvae approach Paramecia in an iterative fashion, juveniles strike from comparatively long distances (Figures 8, 13) and with sufficient precision that their trajectories accurately and quickly strike small targets (Figures 3, 5, 9 and 12).

Larval zebrafish have slow and fast motor systems which manifests as distinct “gaits” for the slow vs. fast/burst swims (Thorsen et al., 2004; Green and Hale, 2012). They depend upon red and white muscle (Buss and Drapeau, 2002) and distinct spinal oscillators or CPGs (Budick and O'Malley, 2000; Buchanan, 2001; Bhatt et al., 2007; McLean et al., 2008). The slow swims used in prey tracking are identical to those used in other larval behaviors (McElligott and O'Malley, 2005) and have been modeled in regards to CPG-frequency modulation (Hill et al., 2005; Kuo and Eliasmith, 2005; Knudsen et al., 2006). The high TBFs seen in early larval strikes are within the range of larval burst swim TBFs (Budick and O'Malley, 2000; Müller and van Leeuwen, 2004; Bhatt et al., 2007; McLean et al., 2008) but gradually decline over the next several weeks (Figure 6C). While the descending commands for predatory vs. other behaviors must differ, parsimony suggests conserved use of slow and fast spinal motor systems given the limited number of spinal interneuron classes seen anatomically (Bernhardt et al., 1990; Hale et al., 2001). These spinal networks could potentially be reconfigured to support the generation of a diverse variety of behaviors (Marder and Bucher, 2007; Bargmann, 2012).

The kinematic diversity of homing strikes (Figure 9) suggests further organizational capability, namely flexible composition of underlying neural commands in relation to the prey's distance and direction. For example, Strike #1 is accomplished by a single slow bend (turn), reflecting an asymmetric motor command. Strike #2 begins with a similarly low-angular velocity turn, but it then transitions into a low TBF forward swim bout, whose controlling neurons remain unknown (but see Green and Hale, 2012). In Strike #2 slow swimming ceases after ~ five cycles, just before the moment of capture. The mechanism for halting in zebrafish is unknown, but based on Xenopus studies might reflect an explicit “halting” command (Perrins et al., 2002), or the run-down of spinal CPG activity after an initial, excitatory forward swim command (Dale, 1998). Inertia allows the juvenile in Strike #2 to coast through the Artemia's location, with suction jaw movements executed about 1080 ms after onset of the episode.

Juvenile Strike #3 has some overlap with Strike #2 in utilizing a command system that produces caudally-propagating bends, but at no time is a conventional slow-swimming pattern seen. Strike #3 contains only 3 bends in total (vs. the 11 bends in Strike #2, and just one bend in Strike #1). Of particular note is the bent posture of the trunk which is held between ~50 and 250 ms post-initiation of the episode. The kinematics suggests that sustained (i.e., non-oscillating) muscle contraction occurs concurrently with propulsive bends that propagate into the caudal trunk. This diversity of homing strikes rules out the use of rote, generic sensorimotor transformations and instead suggests that specific types of commands and command sequences are selected as a motor package based on the exigencies of each predatory opportunity. Such a process might depend on maturing forebrain structures, including an ancestral basal ganglia found in fishes (Medina and Reiner, 1995; Mueller et al., 2008; Ganz et al., 2012).

The initial prey-tracking and strike maneuvers are not “learned” behaviors, since they are performed with precision on the very first predation attempts of early larvae (Borla et al., 2002; McElligott and O'Malley, 2005; McClenahan et al., 2012), in agreement with observations of other larval fishes (Drost, 1987; Job and Bellwood, 1996). These sensorimotor programs thus constitute a kind of “innate knowledge” of predatory opportunities in that they were learned over evolutionary time, stored in the developmental programs of the zebrafish genome and are expressed through development (Adami et al., 2000; McNamara et al., 2006), aided presumably by ongoing sensory feedback that influences general motor and visual system development. The extent to which transitional behaviors and subsequent homing strikes might be innate is uncertain. We did not observe repetitive efforts to strike at a particular location in the arena. Had such repetition existed, larvae could in principle have utilized error signals and cerebellar learning mechanisms to improve performance, but the paucity of errors in conjunction with variable strike patterns, does not fit with conventional error-correction learning algorithms (Portugues and Engert, 2011; Ahrens et al., 2012). While zebrafish larvae exhibit cerebellar function and associative learning (Aizenberg and Schuman, 2011; Valente et al., 2012), the vanishing number of misses with age, along with good success at a young age (roughly 90% hits at 24 dpf; Figure 12), further suggests that growing zebrafish have either extremely fast sensorimotor learning algorithms or employ a series of innate motor programs that appear sequentially across ontogeny. A hybrid mechanism, whereby innate capabilities amplify larval learning skills, is perhaps most parsimonious.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.