Rows of comb-like or tufted gill rakers in the oral cavity of suspension-feeding fishes (for example, herring, anchovies and tilapia) have been thought to serve as (1) non-porous barriers that direct particle-laden water to the sticky oral roof, where particles are retained as water exits from the oral cavity, (2) conventional dead-end filters that sieve particles from water exiting between rakers, or (3) sticky filters that retain particles encountered by a hydrosol filtration mechanism. Here we present data from computational fluid dynamics and video endoscopy in suspension-feeding fish indicating that the rakers of three distantly related species function instead as a crossflow filter. Particles are concentrated inside the oral cavity as filtrate exits between the rakers, but particles are not retained on the rakers. Instead, the high-velocity crossflow along the rakers carries particles away from the raker surfaces and transports the particles towards the oesophagus. This crossflow prevents particles from clogging the gaps between the rakers, and solves the mystery of particle transport from the rakers to the oesophagus.

Suspension-feeding fishes such as goldfish and whale sharks retain prey without clogging their oral filters, whereas clogging is a major expense in industrial crossflow filtration of beer, dairy foods and biotechnology products. Fishes' abilities to retain particles that are smaller than the pore size of the gill-raker filter, including extraction of particles despite large holes in the filter, also remain unexplained. Here we show that unexplored combinations of engineering structures (backward-facing steps forming d-type ribs on the porous surface of a cone) cause fluid dynamic phenomena distinct from current biological and industrial filter operations. This vortical cross-step filtration model prevents clogging and explains the transport of tiny concentrated particles to the oesophagus using a hydrodynamic tongue. Mass transfer caused by vortices along d-type ribs in crossflow is applicable to filter-feeding duck beak lamellae and whale baleen plates, as well as the fluid mechanics of ventilation at fish gill filaments.

SUMMARY It has been hypothesized that, when engulfing food mixed with inorganic particles during benthic feeding, cyprinid fish use protrusions of tissue from the palatal organ to retain the food particles while the inorganic particles are expelled from the opercular slits. In crossflow filtration, the particle suspension is pumped parallel to the filter surface as filtrate exits through the filter pores, causing the suspension to become more concentrated as it travels downstream along the filter. We used high-speed video endoscopy to determine whether carp Cyprinus carpio use crossflow filtration and/or palatal protrusions during benthic feeding. We found that carp use crossflow filtration to concentrate small food particles in the pharyngeal cavity while expelling small dense inorganic particles through the opercular slits and via spits. Our results suggest that, during feeding on small food particles, palatal protrusions serve a localized chemosensory function rather than a mechanical particle-sorting function. However, palatal protrusions did retain large food particles while large inorganic particles were spit anteriorly from the mouth. We also investigated whether flow is continuous and unidirectional during suspension feeding in carp. As reported previously for ventilation in hedgehog skates and for certain industrial crossflow filtration applications, we observed that flow is pulsatile and bidirectional during feeding. These results have implications for hydrodynamic models of crossflow filtration in suspension-feeding fishes.