The predictive start of hunting archer fish: a flexible and precise motor pattern performed with the kinematics of an escape C-start

Abstract

SUMMARY Once their shots have successfully dislodged aerial prey, hunting archer fish monitor the initial values of their prey's ballistic motion and elicit an adapted rapid turning maneuver. This allows these fish to head straight towards the later point of catch with a speed matched to the distance to be covered. To make the catch despite severe competition the fish must quickly and yet precisely match their turn and take-off speed to the initial values of prey motion. However, the initial variables vary over broad ranges and can be determined only after prey is dislodged. Therefore, the underlying neuronal circuitry must be able to drive a maneuver that combines a high degree of precision and flexibility at top speed. To narrow down which neuronal substrate underlies the performance we characterized the kinematics of archer fish predictive starts using digital high-speed video. Strikingly, the predictive starts show all hallmarks of Mauthner-driven teleost C-type fast-starts, which have previously not been noted in feeding strikes and were not expected to provide the high angular accuracy required. The high demands on flexibility and precision of the predictive starts do not compromise their performance. On the contrary, archer fish predictive starts are among the fastest C-starts known so far among teleost fish, with peak linear speed beyond 20 body lengths s-1, angular speed over 4500 deg. s-1, maximum linear acceleration of up to 12 times gravitational acceleration and peak angular acceleration of more than 450 000 deg. s-2. Moreover, they were not slower than archer fish escape C-starts, elicited in the same individuals. Rather, both escapes and predictive starts follow an identical temporal pattern and all kinematic variables of the two patterns overlap. This kinematic equivalence strongly suggests that archer fish recruit their C-start escape network of identified reticulospinal neurons, or elements of it, to drive their predictive starts. How the network drives such a rather complex behavior without compromising speed is a wide open question.

Precision of archerfish C-starts is fully temperature-compensated

“…To ensure that the C-starts were selected solely on the basis of information on prey motion but not on the basis of the responses of the other fish, we analysed only the C-start of the fish that responded first, as described previously (e.g. Rossel et al, 2002;Wöhl and Schuster, 2007;Schlegel and Schuster, 2008). To ensure that accuracy was not due to additional mechanosensory input from the splashing impact of prey, all analyses (including the take-off part that immediately followed the C-start) exclusively relate to C-starts after which the fish took off before the prey's impact.…”

“…The duration of the two stages has previously been shown to be quite variable and related -among other factors -to the degree of turning (Wöhl and Schuster, 2007). It is therefore important to stress that turn sizes were equally distributed at the three temperatures (Kruskal-Wallis: H=0.03, d.f.=2, P>0.99; see Fig.4B) so that the observed differences in acclimated turn duration are due to temperature and not to the fish making systematically smaller turns at higher temperatures.…”

Pre-start timing information is used to set final linear speed in a C-start manoeuvre

“…An adapted level of take-off speed -large if the distance to the landing point of the prey item is large and little time remains until impact -is attained rapidly and kept constant for at least the first 40 ms subsequent to the C-start (Wöhl and Schuster, 2006;Krupczynski and Schuster, 2013). Moreover, linear speed and acceleration during the C-start correlate with take-off speed (Wöhl and Schuster, 2007). Although these findings clearly demonstrate a role of the C-start manoeuvre for setting take-off speed, they do by no means rule out the possibility that post-start fin strokes, which can set in right after the C-start, contribute to or even play a major role in the fine-tuning of post-C-start speed.…”

“…Once a dislodged prey item starts its ballistic path towards the water surface, archerfish are able to determine the later impact point merely on the basis of a brief glimpse of the initial motion of the falling prey (e.g. Rossel et al, 2002;Wöhl and Schuster, 2007;Schlegel and Schuster, 2008;Schuster, 2012;Krupczynski and Schuster, 2013). After a very short latency in the range of 40-100 ms (e.g.…”

“…After a very short latency in the range of 40-100 ms (e.g. Rossel et al, 2002;Schlegel and Schuster, 2008), they elicit their predictive starts, C-starts that turn the fish in the direction of the future landing point of their (still falling) prey (Wöhl and Schuster, 2007). To select the appropriate C-start based on the initial movement of prey, the fish do not need any prior information.…”