Schooling fish under attack are not all equal: some lead, others follow

Abstract

Animal groups such as fish schools, bird flocks and insect swarms appear to move so synchronously that they have long been considered egalitarian, leaderless units. In schooling fish, video observations of their spatial-temporal organization have, however, shown that anti-predator manoeuvres are not perfectly synchronous and that individuals have spatial preferences within the school. Nonetheless, when facing life-or-death situations, it is not known whether schooling fish react to a threat following a random or a hierarchically-based order. Using high-speed video analysis, here we show that schooling fish (Golden grey mullet, Liza aurata) evade a threat in a non-random order, therefore individuals that are first or last to react tend to do so repeatedly over sequential stimulations. Furthermore, startle order is strongly correlated with individual positional preferences. Because school members are known to follow individuals that initiate a manoeuvre, early responders are likely to exert the strongest influence on the escape strategy of the whole school. Our results present new evidence of the intrinsic heterogeneity among school members and provide new rules governing the collective motion of gregarious animals under predator attack.

Figure 1. Experimental setup.

Experimental tank in which schooling fish were startled by the stimulus released by an electromagnet and recorded using a high-speed camera positioned above the tank. The contact between stimulus and water surface was reflected by a mirror and recorded by the camera. The field of view of the camera is represented by the area delimited by broken lines.

Figure 2. Fish show a non-random startle order.

(A) Example of an experimental block, defined as a series of ten trials (ten successive stimulations of the same school). Numbers in italics indicate SO of a given fish in a given trial (e.g. in trial #1, fish A is the 4^th individual to react). (B) Individual fish tended to retain similar startle orders through 10 successive escape responses. Examples of a fast (filled symbols, continuous line) and a slow reacting fish (open symbols, dotted line) within a school. (C) The SO_Exp-M distribution (black columns, N = 70) showed a statistically wider variance than all of the SO_Rand-M distributions [grey columns represent the mean ± S.E. of the ten simulations of SO_Rand-M (N = 70 for each simulation)] and the SO_MC distribution (dark line, N = 20000).

Figure 3. Fish positions within a school.

Top view of a school of 10 fish. (A) Individuals were numbered according to their position relative to the orientation of the school (O_s, indicated by the frontal filled arrow). Fish in the first half of the school (position 1 to 5) were considered to be in the front, while fish in the second half of the school (position 6 to 10) were considered to be in the back. (B) a fish was considered to be at the edge of the school if its tip of the head was at the vertex of the smallest convex polygon enclosing the entire school (1). (C) The four sectors (front-edge, F–E; front-centre, F–C; back-centre, B–C and; back-edge, B–E) were assigned to individuals of the school according to the definitions given for Figures 3A and 3B.

Figure 4. The relationship between mean startle order (SO_Exp-M) and fish positional tendencies within the school.

The mean startle order depended on the positional tendencies of each individual fish at the time of stimulation. The X- and Z-axes correspond to the % of events in which each individual was in the front and at the edge of the school, respectively. Fish in the frontal and central positions react earlier than fish in the back and at the edge of the school. SO_Exp-M = 4.78+0.036 Ep_Exp − 0.029 Fp_Exp; p<0.001, R² = 0.38; N = 70.