Mucus function and crossflow filtration in a fish with gill rakers removed versus intact

Filtration mechanisms are known for only two species of suspension-feeding tilapia, each of which relies on a different method of particle retention. We used high-speed video endoscopy to assess whether a third species of tilapia, Oreochromis aureus, with gill rakers intact as well as surgically removed, uses mucus in the oropharyngeal cavity for hydrosol filtration or uses crossflow filtration to retain particles during suspension feeding. Although a large amount of mucus was visible during feeding with rakers intact, particles were rarely retained in the mucus. The hypothesis that the presence of mucus results in particle entrapment by hydrosol filtration is rejected for O. aureus. Rather than functioning as a sticky filter, mucus is proposed to function in this species to regulate the loss of water between the rakers and between the anterior branchial arches, increasing crossflow speed and thereby increasing the inertial lift force that transports particles radially away from the arches. Gill raker removal resulted in an almost complete lack of observable mucus in the oropharyngeal cavity, probably due to the removal of mucus-secreting cells attached to the gill rakers. However, endoscopic videotapes showed that crossflow filtration continued to operate in the absence of gill rakers and mucus, indicating that the surfaces of the branchial arches play an important role in crossflow filtration

Feeding mechanisms in carp: crossflow filtration, palatal protrusions and flow reversals

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

Convergent and Alternative Designs for Vertebrate Suspension Feeding

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Intra-oral flow patterns and speeds in a suspension-feeding fish with gill rakers removed versus intact

Oreochromis aureus, a species of tilapia, is a suspension-feeding fish that employs a pumping action to bring water into its mouth for filtering.To address questions about water flow inside the mouth, we used a microthermistor flow probe to determine the speed of intra-oral flow during suspension feeding in this species before and after surgical removal of gill rakers. Synchronization with high-speed external videotapes of the fish and high-speed video endoscopy inside the oropharyngeal cavity allowed the first correlation of oral actions with intra-oral flow patterns and speeds during feeding. This analysis established the occurrence of a brief reversal of flow (≈80-ms duration) from posterior to anterior in the oropharyngeal cavity prior to every feeding pump (250–500-ms duration). In industrial crossflow filtration, oscillating or pulsatile flow increases filtration performance by enhancing the back-migration of particles from the region near the filter surface to the bulk flow region, thus reducing particle accumulation that can clog the filter. In endoscopic videotapes, these pre-pump reversals, as well as post-pump reversals (≈500-ms duration), were observed to lift mucus and particles from the branchial arches for subsequent transport toward the esophagus. Intra-oral flow speeds were reduced markedly after removal of the gill rakers. We hypothesize that the decrease in crossflow speed during feeding pumps following the removal of gill rakers and mucus could be due to increased loss of water between the anterior branchial arches

Particle retention in suspension-feeding fish after removal of filtration structures

The suspension-feeding cichlids Oreochromis aureus (blue tilapia) and Oreochromis esculentus (ngege tilapia) are able to selectively retain small food particles. The gill rakers and microbranchiospines of these species have been assumed to function as filters. However, surgical removal of these oral structures, which also removed associated mucus, did not significantly affect the total number of 11–200 μm particles ingested by the fish. This result supports the hypothesis that the branchial arch surfaces themselves play an important role in crossflow filtration. Both species selectively retained microspheres greater than 50 μm with gill rakers and microbranchiospines intact as well as removed, demonstrating that neither these structures nor mucus are necessary for size selectivity to occur during biological crossflow filtration. After removal of the gill rakers and microbranchiospines, O. esculentusretained significantly more microspheres 51–70 μm in diameter and fewer 91–130 μm microspheres compared to retention with intact structures, but the particle size selectivity of O. aureus was not affected significantly. These results support conclusions from previous computational fluid dynamics simulations indicating that particle size can have marked effects on particle trajectory and retention inside the fish oropharyngeal cavity during crossflow filtration. The substantial inter-individual variability in particle retention by suspension-feeding fish is an unexplored area of research with the potential to increase our understanding of the factors influencing particle retention during biological filtration

Integration of swimming kinematics and ram suspension feeding in a model American paddlefish, Polyodon spathula

Ram suspension-feeding fishes swim with an open mouth to force water through the oral cavity and extract prey items that are too small to be pursued individually. Recent research has indicated that, rather than using a dead-end mechanical sieve, American paddlefish (Polyodon spathula) employ vortical cross-step filtration. In this filtration mechanism, vortical flow that is generated posterior to the branchial arches organizes crossflow filtration processes into a spatial structure across the gill rakers. Despite the known impact of locomotor kinematics on fluid flow around the bodies of swimming fish, the effects of locomotor kinematics on filtration mechanisms in ram suspension feeders are unknown. Potential temporal organization of filtration mechanisms in ram suspension-feeding fish has not been studied previously. We investigated the effects of locomotor kinematics associated with undulatory swimming on intra-oral flow patterns and food particle transport. A mechanized model of the oral cavity was used to simulate the swimming kinematics of suspension-feeding paddlefish. We recorded fluctuations of flow speed and pressure within the model, which occurred at a frequency that corresponded with the frequency of the model\u27s strides. Using the mechanized model in a flow tank seeded with Artemia cysts, we also showed that swimming kinematics aided the transport of this simulated food to the posterior margins of the gill slots, although the time scale of this transport is expected to vary with prey parameters such as size and concentration. Dye stream experiments revealed that, although stable vortical flow formed because of flow separation downstream of backward-facing steps in control trials, vortical flow structures in mechanized trials repeatedly formed and shed. These findings suggest strong integration between locomotor and feeding systems in ram suspension-feeding fishes

Separating oil from water: suspension-feeding goldfish ingest liquid vegetable oil

We show that goldfish (Carassius auratus) voluntarily ingest liquid canola oil at the surface of the water and can swallow significant quantities of oil. The ability of fish to separate floating oil from water has not been tested previously, and the mechanisms used to retain oil in the form of suspended droplets, globules, or a surface film are unknown. Chromatograms of fatty acid methyl esters (FAMEs) prepared from gut samples confirmed that goldfish were able to obtain a substantial proportion of their daily lipid intake from canola oil at the surface of laboratory aquaria. Quantification of goldfish suspension-feeding, processing, and spitting behavior suggested that upper jaw protrusion with a closed mouth during processing was important for the handling of different food types, including oil. Crossflow filtration and the generation of vortices could be involved in oil retention by goldfish, as these processes are used industrially to separate oil from water. These results have implications for the uptake of hydrophobic pollutants and dietary lipids at the surface by suspension-feeding fishes

Particle separation mechanisms in suspension-feeding fishes: key questions and future directions

Key unresolved questions about particle separation mechanisms in suspension-feeding fishes are identified and discussed, focusing on areas with the potential for substantial future discovery. The published hypotheses that are explored have broad applicability to biological filtration and bioinspired improvements in commercial and industrial crossflow microfiltration processes and microfluidics. As the first synthesis of the primary literature on the particle separation mechanisms of marine, estuarine, and freshwater suspension-feeding fishes, the goals are to enable comparisons with invertebrate suspension-feeding processes, stimulate future theoretical and empirical studies, and further the development of biomimetic physical and computational fluid dynamics models. Of the eight particle separation mechanisms in suspension-feeding fishes, six have been proposed within the past twenty years (inertial lift and shear-induced migration, reduction of effective gap size by vortices, cross-step filtration, vortical flow along outer faces of gill raker plates, ricochet filtration, and lateral displacement). The pace of discovery is anticipated to continue accelerating. Multidisciplinary collaboration and integration among biologists and engineers (including chemical, mechanical, biomedical, and filtration engineering) will result in new perspectives to identify patterns and potential unifying mechanisms across the breadth of suspension-feeding fish taxa, morphology, and function

Fish mouths as engineering structures for vortical cross-step filtration

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\u27 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

Paddlefish buccal flow velocity during ram suspension feeding and ram ventilation

A micro-thermistor probe was inserted into the buccal cavity of freely swimming paddlefish to measure flow velocity during ram ventilation, ram suspension feeding and prey processing. Swimming speed was measured from videotapes recorded simultaneously with the buccal flow velocity measurements. Both swimming velocity and buccal flow velocity were significantly higher during suspension feeding than during ram ventilation. As the paddlefish shifted from ventilation to feeding, buccal flow velocity increased to approximately 60 % of the swimming velocity. During prey processing, buccal flow velocity was significantly higher than the swimming velocity, indicating that prey processing involves the generation of suction. The Reynolds number (Re) for flow at the level of the paddlefish gill rakers during feeding is about 30, an order of magnitude lower than the Re calculated previously for pump suspension-feeding blackfish. These data, combined with data available from the literature, indicate that the gill rakers of ram suspension-feeding teleost fishes may operate at a substantially lower Re than the rakers of pump suspension feeders