Abstract

Although the motor control of feeding is presumed to be generally conserved, some fishes are capable of modulating the feeding behaviour in response to prey type and or prey size. This led to the 'feeding modulation hypothesis', which states that rapid suction strikes are pre-programmed stereotyped events that proceed to completion once initiated regardless of sensory input. If this hypothesis holds true, successful strikes should be indistinguishable from unsuccessful strikes owing to a lack of feedback control in specialized suction feeding fishes. The hydrodynamics of suction feeding in white-spotted bamboo sharks (Chiloscyllium plagiosum) was studied in three behaviours: successful strikes, intraoral transports of prey and unsuccessful strikes. The area of the fluid velocity region around the head of feeding sharks was quantified using time-resolved digital particle image velocimetry (DPIV). The maximal size of the fluid velocity region is 56% larger in successful strikes than unsuccessful strikes (10.79 cm2 vs 6.90 cm2), but they do not differ in duration, indicating that strikes are modulated based on some aspect of the prey or simply as a result of decreased effort on the part of the predator. The hydrodynamic profiles of successful and unsuccessful strikes differ after 21 ms, a period probably too short to provide time to react through feedback control. The predator-to-prey distance is larger in missed strikes compared with successful strikes, indicating that insufficient suction is generated to compensate for the increased distance. An accuracy index distinguishes unsuccessful strikes (-0.26) from successful strikes (0.45 to 0.61). Successful strikes occur primarily between the horizontal axis of the mouth and the dorsal boundary of the ingested parcel of water, and missed prey are closer to the boundary or beyond. Suction transports are shorter in duration than suction strikes but have similar maximal fluid velocity areas to move the prey through the oropharyngeal cavity into the oesophagus (54 ms vs 67 ms).

Highlights

  • In spite of this conservatism, most of these fishes are capable of modulating the kinematics of the feeding behaviour in response to prey type, prey size or stage (Moss, 1972; Liem, 1978; Lauder, 1981; Frazzetta and Prange, 1987; Motta et al, 1997; Nemeth, 1997a; Nemeth, 1997b; Ferry-Graham, 1998; Wilga and Motta, 1998a; Wilga and Motta, 1998b; Wilga and Motta, 2000; Friel and Wainwright, 1998; Pretlow-Edmonds, 1999; Ferry-Graham et al, 2001)

  • Technological advances in measuring fluid flow have resulted in a recent upsurge of studies on the hydrodynamics of suction feeding in fishes (Higham et al, 2006a; Higham et al, 2006b; Nauwelaerts et al, 2007)

  • Specialized suction or ram feeding shark species exhibit shorter durations and less modulatory ability than more generalized taxa that use a combination of these behaviours (Motta and Wilga, 2001)

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Summary

Introduction

Motor control of the feeding mechanism is typically regarded as phylogenetically conserved in fishes as neuromuscular patterns are similar among diverse species (Wainwright et al, 1989; Friel and Wainwright, 1998; Lauder and Shaffer, 1993; Wilga and Motta, 1998a; Wilga and Motta, 1998b; Wilga and Motta, 2000; Wilga et al, 2000; Grubich, 2001; Wainwright, 2002) (see Wilga et al, 2001). Specialized suction or ram feeding shark species exhibit shorter durations and less modulatory ability than more generalized taxa that use a combination of these behaviours (Motta and Wilga, 2001) These observations led to the ‘feeding modulation hypothesis’, which states that rapid suction strikes are pre-programmed and stereotyped events that proceed to completion once initiated regardless of sensory input (Motta and Wilga, 2001). If this hypothesis holds true, once initiated, the hydrodynamics of successful strikes should be indistinguishable from those of unsuccessful strikes owing to a lack of feedback control

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