Injury-mediated decrease in locomotor performance increases predation risk in schooling fish

Abstract

The costs and benefits of group living often depend on the spatial position of individuals within groups and the ability of individuals to occupy preferred positions. For example, models of predation events for moving prey groups predict higher mortality risk for individuals at the periphery and front of groups. We investigated these predictions in sardine (Sardinella aurita) schools under attack from group hunting sailfish (Istiophorus platypterus) in the open ocean. Sailfish approached sardine schools about equally often from the front and rear, but prior to attack there was a chasing period in which sardines attempted to swim away from the predator. Consequently, all sailfish attacks were directed at the rear and peripheral positions of the school, resulting in higher predation risk for individuals at these positions. During attacks, sailfish slash at sardines with their bill causing prey injury including scale removal and tissue damage. Sardines injured in previous attacks were more often found in the rear half of the school than in the front half. Moreover, injured fish had lower tail-beat frequencies and lagged behind uninjured fish. Injuries inflicted by sailfish bills may, therefore, hinder prey swimming speed and drive spatial sorting in prey schools through passive self-assortment. We found only partial support for the theoretical predictions from current predator-prey models, highlighting the importance of incorporating more realistic predator-prey dynamics into these models.This article is part of the themed issue 'Physiological determinants of social behaviour in animals'.

Keywords: fish schools; group-living; locomotion; predation; spatial positions.

Figure 1.

Micro-CT image of a 5 cm bill-tip showing (a) the dorsal surface with curved micro-teeth and (b) a cross-section with micro-teeth mainly on the sides of the bill. Sailfish bills were scanned on a Skyscan 1172 (Brucker-CT, Kontich, Belgium) with an effective pixel size of 7 µm, an energy of 65 KeV, 360° scans using an Al filter 500 µm thick. Reconstruction was performed using manufacturer software (NRecon v. 1.6.9.4) and data were visualized (CTvox) and further processed using Fiji [22].

Figure 2.

(a) Still-frame image taken from one of the videos showing the white injury marks on the sardines caused by damage from sailfish bills. Markings show the front, rear and two sides of the school. Dashed line shows the division between front and rear half of the school. The original image has its contrast and brightness adjusted; (b) before binary thresholding; (c) which reveals the positions of the injuries on the fish in the front and rear halves. (d) The number of pixels indicating injury in the front and rear halves of schools. Data points are jittered to reveal overlapping data points. Boxplots show median, interquartile ranges and whiskers show highest and lowest values (excluding outliers).

Figure 3.

(a,b) Observed frequency of hits and captures for different school positions; front versus rear half (hits: 30 versus 2, captures: 34 versus 0) of the school and periphery versus centre (hits: 25 versus 0, captures: 35 versus 0).

Figure 4.

Comparison of TBFs of injured and uninjured fish in the front (N = 30) and rear half (N = 52) of the sardine schools. Data points are jittered to reveal overlapping data points. Boxplots show median, interquartile ranges and whiskers show highest and lowest values (excluding outliers).