Schooling Fish from a New, Multimodal Sensory Perspective

Abstract

The acoustic hypothesis suggests that schooling can result in several benefits. (1) The acoustic pattern (AP) (pressure waves and other water movements) produced by swimming are likely to serve as signals within fish shoals, communicating useful spatial and temporal information between school members, enabling synchronized locomotion and influencing join, stay or leave decisions and shoal assortment. (2) Schooling is likely to reduce the masking of environmental signals, e.g., by auditory grouping, and fish may achieve windows of silence by simultaneously stopping their movements. (3) A solitary swimming fish produces an uncomplicated AP that will give a nearby predator's lateral line organ (LLO) excellent information, but, if extra fish join, they will produce increasingly complex and indecipherable APs. (4) Fishes swimming close to one another will also blur the electrosensory system (ESS) of predators. Since predators use multimodal information, and since information from the LLO and the ESS is more important than vision in many situations, schooling fish may acquire increased survival by confusing these sensory systems. The combined effects of such predator confusion and other acoustical benefits may contribute to why schooling became an adaptive success. A model encompassing the complex effects of synchronized group locomotion on LLO and ESS perception might increase the understanding of schooling behavior.

Keywords: electrosensory system; evolution; lateral line organ; predator confusion.

Figure 1

The black spot in the middle is a small fish emitting sound and water movements during locomotion while swimming close to a predator with a lateral line organ. Vibrations, swimming animals, breathing, vocalizations and other mechanical disturbances will generate a steep pressure gradient close to the source, giving rise to a net flow of water. This water flow will obscure particle compressions and rarefactions; as a consequence, near the source, water movements will be more powerful than the propagated pressure wave. These pressure changes are perceived both by the lateral line system and the inner ear. The lateral line, with many densely grouped sampling points, requires a steep spatial gradient for stimulation, but, accordingly, it will be able to resolve that gradient in spatial detail. The auditory system may react to a similar pressure gradient by integrating the differences in pressure along the contralateral sides of its body, but the inner ear cannot resolve spatial details of the stimulus field [25]. Isopressure curves were modelled through dipole flow equations [26].

Figure 2

The risk of being eaten by nearby fish may have contributed to evolutionary change towards shoals with individuals of similar size. It is likely that advancement of the OLS was fundamental in the start of predatory behavior [38,44]; moreover (and consequently), this would have increased the risk of being detected and eaten by a larger fish. Conversely, the OLS would have supported small fish to detect and avoid bigger fish. The figure is reproduced from [30] with permission from Current Zoology.

Figure 3

Because of cannibalism, fish may have developed a predisposition to join fish of similar size. Fish of comparable size and body shape will emit similar hydrodynamic signals; such incidental sound of locomotion may be useful in JLS decisions, which may contribute to shoal homogeneity. The figure is reproduced from [30] with permission from Current Zoology.

Figure 4

The white, black and gray circles represent small prey fish swimming close to a larger predatory fish (gray). Since the prey fishes are closely situated, the hydrodynamic signals they produce will overlap. Increasing the number and/or reducing the distance between prey fishes will create more overlapping and, thus, more complex signals. This may result in significant predator confusion in regard to the OLS system. The figure is reproduced from [31] with kind permission from Fish and Fisheries, Wiley-Blackwell, Hoboken, New Jersey, U.S.

Figure 5

The predatory fish (red) uses the electrosensory system to detect and distinguish electrical fields of prey. (A) An isolated fish is easy to detect and localize. (B) In a school, the individual fish is difficult to perceive, since the “electrical landscape” is more complicated. Prey fish (yellow) must be about five body widths apart to produce separate signals, or else they will form a blurred image [87]. The figure is reproduced from [30] with permission from Current Zoology.