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Multisensory Integration and Behavioral Plasticity in Sharks from Different Ecological Niches

Figure 1

Sensory signals and their use by hunting sharks.

Senses are indicated by capital letters (e.g. V = vision); asterisk (e.g. V*) denotes sense used to measure and orient to the bulk flow (i.e., by detecting environment features); no asterisk (e.g. V) denotes sense used to process prey cues; slashed (e.g. ) indicates sensory block. Background colors in A, B, and C indicate areas of signal availability corresponding to signal dispersal fields in A. Behavioral phases in boxes occur at a discrete distance from the source; behavioral phases in boxed arrows occur over a distance; line arrows indicate transitions from one phase of the behavior to the next. A. Physical model of prey signal fields (After [1]). Prey emit a complex mixture of sensory stimuli that radiate and disperse into the habitat. Animals can detect the bulk flow vector (arrow) by measuring their drift along the walls and substrate, using vision (V*) or touch (T*) of the walls or bottom, or, by detecting turbulence in the bulk flow, with the lateral line (L). Bulk flow disperses prey odor downstream over large distances where it can be detected by olfaction (O, green); closer to the source, prey-generated wake turbulence becomes detectable by the lateral line (L, purple). Close to the source, the prey becomes directly detectable based on vision (V, red), lateral line imaging of the acoustic near field (L, delineated by purple dotted line), electroreception (E, orange), and touch (T, direct tactile contact with prey). B. The blacktip shark, Carcharhinus limbatus. From downstream, the blacktip shark detects the presence of prey using O and, during the daytime, tracks the bulk flow upstream using OV* or OL. Seeing the prey, it switches to V to orient and strike from a distance (∼2 m). Near the prey, the strike is adjusted using L. Then it switches to E to ram-capture the prey. With the lateral line blocked () it often misses the prey; successful captures involve increased ram. If , it can capture prey using T; if , it will miss. When approaching prey from downstream at night (under moonless conditions; ), it detects (O) and tracks (OL) the prey until it is at close range (∼20 cm), then orients and strikes using L, but captures using less ram. If , it detects the prey (O), but cannot track and ceases to feed. When approaching prey from upstream (), it detects the prey using V and orients, strikes, and captures. If it approaches the prey from upstream at night (), it will not detect the prey and will not feed. C. The bonnethead, Sphyrna tiburo. From downstream, the bonnethead detects prey using O and, during the daytime, tracks it using OV* or OL; it switches to V to orient and strike, but does so at a closer range (∼1 m) than the blacktip shark, then switches to E to capture using ram-biting. When approaching prey from downstream at night (), it detects (O) and tracks the prey (OL), but cannot orient or strike and ceases to feed. If , it detects prey (O), but cannot track, and ceases to feed. When approaching prey from upstream (), it detects prey using V, then orients, strikes, and captures. At night (), it detects (O) and tracks (OL) prey, but cannot orient and strike and ceases to feed. If , it misses the prey even when touching it (T or ). D. The nurse shark, Ginglymostoma cirratum. From downstream, the nurse shark detects prey using O, then, during the daytime, tracks using OV*, OL, or OT*. At a close range it switches to V, L, or E to orient and strike, then switches to E to suction-capture the prey. At night (), it detects (O), tracks (OL or OT*), orients and strikes (L or E) as above, but modulates its capture by increasing suction and decreasing ram. When approaching prey from upstream (), it does not detect the prey and does not feed. Like the blacktip shark, if , it can still capture the prey if it touches it (T), but it misses when it does not touch () the prey. Nurse shark illustration copyright José Castro, with permission. Pinfish, shrimp, bonnethead, and blacktip shark illustrations copyright Diane Peebles, with permission.

Figure 1

doi: https://doi.org/10.1371/journal.pone.0093036.g001