Mechanics of ventilation in swellsharks, Cephaloscyllium ventriosum (Scyliorhinidae)

Abstract

A simple two-pump model has served to describe the mechanics of ventilation in cartilaginous and bony fishes since the pioneering work of G. M. Hughes. A hallmark of this model is that water flow over the gills is continuous. Studies of feeding kinematics in the swellshark Cephaloscyllium ventriosum, however, suggested that a flow reversal occurred during prey capture and transport. Given that feeding is often considered to be simply an exaggeration of the kinematic events performed during respiration, I investigated whether flow reversals are potentially present during respiration. Pressure and impedance data were coupled with kinematic data from high-speed video footage and dye studies and used to infer patterns of water flow through the heads of respiring swellsharks. Swellsharks were implanted with pressure transducers to determine the pattern and magnitude of pressures generated within the buccal and parabranchial (gill) cavities during respiration. Pressure traces revealed extended periods of pressure reversal during the respiratory cycle. Further, impedance data suggested that pressures within the buccal and parabranchial cavities were not generated by the cyclic opening and closing of the jaws and gills in the manner previously suggested by Hughes. Thus, the classic model needs to be re-evaluated to determine its general applicability. Two alternative models for pressure patterns and their mechanism of generation during respiration are provided. The first depicts a double-reversal scenario common in the swellshark whereby pressures are reversed following both of the pump stages (the suction pump and the pressure pump) rather than after the pressure-pump stage only. The second model describes a scenario in which the suction pump is insufficient for generating a positive pressure differential across the gills; thus, a pressure reversal persists throughout this phase of respiration. Kinematic analysis based on high-speed video footage and dye studies, however, suggested that during respiration, as opposed to feeding, distinct flow reversals do not result from the pressure reversals. Thus, water is probably pooling around the gill filaments during the long periods of pressure reversal.