Social familiarity improves fast-start escape performance in schooling fish

Abstract

Using social groups (i.e. schools) of the tropical damselfish Chromis viridis, we test how familiarity through repeated social interactions influences fast-start responses, the primary defensive behaviour in a range of taxa, including fish, sharks, and larval amphibians. We focus on reactivity through response latency and kinematic performance (i.e. agility and propulsion) following a simulated predator attack, while distinguishing between first and subsequent responders (direct response to stimulation versus response triggered by integrated direct and social stimulation, respectively). In familiar schools, first and subsequent responders exhibit shorter latency than unfamiliar individuals, demonstrating that familiarity increases reactivity to direct and, potentially, social stimulation. Further, familiarity modulates kinematic performance in subsequent responders, demonstrated by increased agility and propulsion. These findings demonstrate that the benefits of social recognition and memory may enhance individual fitness through greater survival of predator attacks.

Fig. 1. Components of the fast-start escape response.

This study examined the role of social familiarity in the reaction timing and kinematic performance of schools of the tropical damselfish Chromis viridis, focusing on three key traits: latency, average turning rate, and distance covered. a Latency indicates the time period between the threatening stimulus breaking the water surface and the fish’s first movement, with a shorter latency indicating a faster reaction time. b Average turning rate is measured by dividing the angle achieved during the first unilateral bend of the reaction (i.e. stage 1) by the duration of time to achieve that angle, with a higher turning rate indicating greater agility in the response. c Distance covered indicates the distance moved during the first 42 ms of the reaction, the mean time period for individuals to complete two body bends (i.e. stages 1 and 2), and is indicative of the response’s speed and acceleration. In all panels a–c, the grey fish silhouette indicates the fish’s position immediately prior to stimulation and the black fish indicates the fish’s position during each component of the fast-start escape response.

Fig. 2. The latency of the fast-start escape response in familiar versus unfamiliar schools of the damselfish Chromis viridis.

Frequency histograms of response latencies for first responders (a) and subsequent responders (b). c Response latencies by responder number, the sequential order of latencies in each fish’s respective group. Each larger dot represents the mean ± s.e. (y axis logged for illustration), with small dots indicative of individual data points. p-values indicate results of the generalised linear model (a) and linear mixed-effects model (b, c) analyses (n = 24 schools, composed of 8 fish each).

Fig. 3. The average turning rate of the fast-start escape response in familiar versus unfamiliar schools of the damselfish Chromis viridis.

a Average turning rate by responder number (which denotes the sequential order of responses in each fish’s respective group). Each larger dot represents the mean ± s.e., with small dots indicative of individual data points. p-values indicate results of linear mixed-effects model analyses (n = 24 schools, composed of 8 fish each). b Typical escape responses in the familiar (left) and unfamiliar (right) treatments. Lines represent the fish midline and arrows indicate the location of the head in successive frames at 4.2 ms intervals. The greater number of lines in the unfamiliar example indicates that the individual took more time to achieve a similar evasive manoeuvre to the individual in the familiar treatment.

Fig. 4. The distance covered during the fast-start escape response in familiar versus unfamiliar schools of the damselfish Chromis viridis.

Distance covered (i.e. the distance moved during the first 42 ms of the reaction, the mean time period for individuals to complete two body bends known as stages 1 and 2) by responder number (the sequential order of responses in each fish’s respective group). This trait is indicative of the escape response’s speed and acceleration (n = 24 schools, composed of 8 fish each). Each larger dot represents the mean ± s.e., with small dots indicative of individual data points.

Fig. 5. Effect of familiarity on escape performance of fish schools (Chromis viridis).

a Nearest neighbour distance (NND) denotes the distance to the closest neighbour (mm). b School area indicates the school’s horizontal spread (cm²). c Alignment is a measure of the variation in the orientation of all school members. This variable is characterised by the length of the mean circular vector (r). Each larger dot represents the mean ± s.e., with small dots indicative of individual data points (n = 24 schools, composed of 8 fish each).

Fig. 6. Example school behaviour after stimulation.

Each arrow shows the position and orientation of one fish. Successive frames from top to bottom illustrate the school’s cohesion and alignment at 0 ms (the moment immediately before stimulation), +20 ms (during the escape response), and +100 ms (following the escape response) post-stimulation. The experimental arena measured 50 cm (long) × 40 cm (wide), with directional flow from right to left in the illustration. Both illustrated schools were stimulated by the right lateral stimulus, with an identical lateral stimulus on the left side of the arena, relative to the directional flow (both 2 cm from each of the lateral walls in the centre of the swim tunnel). To control for a stimulus side preference, the use of the left or right lateral stimulus was alternated between trials.