S. Laurie Sanderson

Crossflow filtration in suspension-feeding fishes

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.

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

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.

Development and Evolution of Aquatic Larval Feeding Mechanisms

Publisher Summary This chapter discusses the development and evolution of feeding mechanisms in aquatic larval vertebrates, such as fishes and amphibians. Fish larva is the immature life-history stage that differs morphologically from the juvenile and adult. The time between hatching and metamorphosis may range from a few days in tropical fish species, to a few weeks or months in most temperate fishes, to years in the eel Anguilla. In amphibians, the larval stage begins at hatching, when an embryo escapes from its egg capsule. Larvae are morphologically distinct from adults and are not reproductive. Fish larvae undergo trophic ontogeny as their diet changes markedly with growth. Four types of nutrient acquisitions are recognized in fish larvae: endogenous, absorptive, mixed, and exogenous. For the embryos of oviparous and ovoviviparous fishes, yolk platelets and oil globules serve as the primary source of nutrition. Many marine invertebrate larvae are capable of supplementing their nutrition by the uptake of dissolved organic matter (DOM) via transepidermal transport. Mixed feeding refers to any combination of endogenous, absorptive, and exogenous feeding, and occurs as concurrent endogenous and exogenous feeding during the time between first exogenous feeding and complete resorption of the yolk sac.

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.

Evidence for ram suspension feeding by the piscivore, Seriola dumerili (Carangidae)

SynopsisWe have quantitatively analyzed a videotape of Seriola dumerili (Carangidae) displaying ram suspension-feeding behavior and ram ventilation in the field. This is the first report of facultative suspension feeding by a piscivorous carangid. The intraoral morphology of S. dumerili is not typical of ram suspension-feeding fishes in that closely-spaced, long gill rakers are lacking. While the mechanism of particle retention is not known for any ram suspension-feeding fish species, scanning electron microscopy revealed denticles on the branchial surfaces of S. dumerili that could play a role in particle entrapment.

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. esculentus retained 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.

Physical modeling of vortical cross-step flow in the American paddlefish, Polyodon spathula

Vortical cross-step filtration in suspension-feeding fish has been reported recently as a novel mechanism, distinct from other biological and industrial filtration processes. Although crossflow passing over backward-facing steps generates vortices that can suspend, concentrate, and transport particles, the morphological factors affecting this vortical flow have not been identified previously. In our 3D-printed models of the oral cavity for ram suspension-feeding fish, the angle of the backward-facing step with respect to the model’s dorsal midline affected vortex parameters significantly, including rotational, tangential, and axial speed. These vortices were comparable to those quantified downstream of the backward-facing steps that were formed by the branchial arches of preserved American paddlefish in a recirculating flow tank. Our data indicate that vortices in cross-step filtration have the characteristics of forced vortices, as the flow of water inside the oral cavity provides the external torque required to sustain forced vortices. Additionally, we quantified a new variable for ram suspension feeding termed the fluid exit ratio. This is defined as the ratio of the total open pore area for water leaving the oral cavity via spaces between branchial arches that are not blocked by gill rakers, divided by the total area for water entering through the gape during ram suspension feeding. Our experiments demonstrated that the fluid exit ratio in preserved paddlefish was a significant predictor of the flow speeds that were quantified anterior of the rostrum, at the gape, directly dorsal of the first ceratobranchial, and in the forced vortex generated by the first ceratobranchial. Physical modeling of vortical cross-step filtration offers future opportunities to explore the complex interactions between structural features of the oral cavity, vortex parameters, motile particle behavior, and particle morphology that determine the suspension, concentration, and transport of particles within the oral cavity of ram suspension-feeding fish.

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

ABSTRACT 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 models 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. Summary: Yaw and heave generate cyclical flow patterns inside the mouth of a mechanized suspension-feeding fish model, aiding food particle transport.

Effects of prey type on suspension-feeding behavior in Nile tilapia

Quantitative analysis of feeding behavior in the Nile tilapia,Oreochromis niloticus(Linn.), assessed the frequencies and functions of five behaviors (long pumps, short pumps, benthic pumps, reversals, spits) during suspension feeding on four prey types (whole TetraMin flakes, crushed TetraMin flakes, brine shrimp, bacteria). We tested the hypothesis that suspension-feeding behavior is affected by prey type. Long pumps occurred significantly more frequently (p= 0.01) during feeding on bacteria (2–8 ×105 cells ml−1) than on other prey. Short pumps, with a substantially reduced gape and significantly shorter duration (p < 0.0001) relative to long pumps, appeared to separate organic particles from inorganic material such as gravel. Benthic pumps were directed at food that had settled on the substrate, which also resuspended organic particles into the aquarium water due to substrate disturbance. Reversals, shown previously to generate a posterior to anterior water flow within the oral cavity, function both to separate organic from inorganic particles by resuspension within the oral cavity and to transport prey retained in mucus. Spits expelled inorganic material through the mouth, and occurred significantly less frequently (p = 0.04) during feeding on brine shrimp versus whole or crushed flakes. Prey type affects the frequency of specific behaviors for prey collection and processing during suspension feeding, providing insight into the functions of these behaviors.