In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish
Curation statements for this article:-
Curated by eLife
Evaluation Summary:
How do fish suck food underwater? Using new artificial food particles that are radio opaque and naturally buoyant, Provini et al. imaged the roller-coaster ride that food particles make being sucked-in from outside to inside the fish, using 3D stereo high-speed fluoroscopy. The recordings show fish to have an intriguing ability to generate flows that center the food particles as they enter the buccal cavity that carries them from the outside to the center of the digestive tract. Remarkably, the flow patterns in the mouth that accomplish this seem to differ between the two species of fish studied, although samples sizes are small at present. These new insights will interest biologists working on suction feeding mechanisms ranging from millimeter-sized carnivorous water plants, tadpoles and fish larvae, to large fish and marine mammals, and even gigantic whales. Bioinspired engineers designing rapid underwater suction apparatuses may benefit from harnessing the new insights to elegantly center items of interest.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
- Evolutionary Biology (eLife)
Abstract
Virtually all fishes rely on flows of water to transport food to the back of their pharynx. While external flows that draw food into the mouth are well described, how intraoral waterflows manage to deposit food at the esophagus entrance remains unknown. In theory, the posteriorly moving water must, at some point, curve laterally and/or ventrally to exit through the gill slits. Such flows would eventually carry food away from the esophagus instead of toward it. This apparent paradox calls for a filtration mechanism to deviate food from the suction-feeding streamlines. To study this gap in our fundamental understanding of how fishes feed, we developed and applied a new technique to quantify three-dimensional (3D) patterns of intraoral waterflows in vivo. We combined stereoscopic high-speed X-ray videos to quantify skeletal motion (XROMM) with 3D X-ray particle tracking (XPT) of neutrally buoyant spheres of 1.4 mm in diameter. We show, for carp ( Cyprinus carpio ) and tilapia ( Oreochromis niloticus ), that water tracers displayed higher curvatures than food tracers, indicating an inertia-driven filtration. In addition, tilapia also exhibited a ‘central jet’ flow pattern, which aids in quickly carrying food to the pharyngeal jaw region. When the food was trapped at the branchial basket, it was resuspended and carried more centrally by periodical bidirectional waterflows, synchronized with head-bone motions. By providing a complete picture of the suction-feeding process and revealing fundamental differences in food transport mechanisms among species, this novel technique opens a new area of investigation to fully understand how most aquatic vertebrates feed.
Article activity feed
-
-
Author Response:
Reviewer #1:
Suction feeding is recognized as a nearly ubiquitous prey capture mode in fishes, and the hydrodynamics of these flows are reasonably understood. Provoni et al. deal with a role that is as important but much less understood, i.e. the role of these flows in intra-oral prey transport. Specifically, they ask how the flows within the buccal cavity can help transport the prey into the mouth. The major obstacle to understand these flows is that they are internal, so it was difficult to quantify them.
Here, the authors developed and used a technique that enabled tracking of tracer particles that are smaller and less dense than the prey, thereby improving our ability to quantify the flows. They show that the suction flows can be directed towards the esophagus at least in one of the species they used, and that …
Author Response:
Reviewer #1:
Suction feeding is recognized as a nearly ubiquitous prey capture mode in fishes, and the hydrodynamics of these flows are reasonably understood. Provoni et al. deal with a role that is as important but much less understood, i.e. the role of these flows in intra-oral prey transport. Specifically, they ask how the flows within the buccal cavity can help transport the prey into the mouth. The major obstacle to understand these flows is that they are internal, so it was difficult to quantify them.
Here, the authors developed and used a technique that enabled tracking of tracer particles that are smaller and less dense than the prey, thereby improving our ability to quantify the flows. They show that the suction flows can be directed towards the esophagus at least in one of the species they used, and that repeated bidirectional flows can be used to redirect particles trapped at the branchial basket towards the esophagus. In doing so, they highlight the role of the suction flows in transport of food, providing a possible explanation to the ubiquity of suction flows even among fish that don't rely on the external flows to capture their prey.
Quantifying internal flows is a demanding task, and the paper presents new and exciting data. As is typical to new techniques, there are important limitations to its current use. The tracers are larger than those used for particle imaging velocimetry, and are heavier than the water. Therefore, they don't track the water precisely. It is difficult to predict the error generated due to this limitation, because it depends on the velocity gradients in the flow (for example accelerations). Additionally, the number of tracers is limited, so they provide a partial representation of the flows within the mouth. It stands to reason that particles drawn from different locations will have different trajectories, however this is not quantitatively analyzed.
Particle tracking can lend itself to a quantitative analysis of the transport flows, but unfortunately the paper does not take full advantage of these capacities. The intake flow patterns are qualitatively described, and a quantitative estimate of the volume of water that passes near the esophagus are examples for such potential. Other important parameters such as efficiency can be potentially derived directly.
The most important message of the results presented is that the flow of water inside the mouth has a functional role in moving the prey towards the esophagus, and that it can differ between species. These results teach us that the suction flows are important not only to prey capture but also to prey transport.
Thank you for your interesting public review.
In a revised version of the paper, we have evaluated the effect of size and density on tracking performance of our particles using CFD analysis. The results are presented in a new Figure (Figure 8), which is further illustrated by a video (Figure 8 – video 1). It serves to quantify the limitations due to particle size and buoyancy imperfection.
The CFD results reassure that the finite size (1.4 mm diameter) and density (up to about 1050 kg m-3) of the current sample of particles (Figure 7) does not hinder a realistic assessment of the suction flows by fish. A small deviation of the path in the direction of gravity can be expected (Figure 8b), but this should be smaller than 1 mm even for the heaviest particles of 1050 kg m-3. Lag during flow acceleration and overshoot during deceleration for the slightly negatively buoyant particles was relatively small (Figure 8c) and therefore acceptable to describe general patterns of flow during suction feeding.
Reviewer #2:
This is a fascinating study that adds great resolution to the mechanisms of water flow in the mouth of fish during suction feeding. Using high-speed x-ray video (XROMM) to track food items and particles in the water, the authors show convincingly that fish have an intriguing ability to generate flows that center the food at the esophagus, and that intraoral flow differs between species. The video is impressive, showing all the particles flow into the mouth, and separation to direct food to the gullet and water to the outflow exit (gill arches).
The methods of XROMM and particle tracking are quite well known -- there is nothing new in either approach, nor in combining them to track the prey item. However, the authors created a new kind of marker to enable tracking water flow patterns; a bead surrounded by foam, to create neutral buoyancy, that worked really well. Overall a fascinating study that adds to our understanding of suction feeding in fish.
Thank you for your nice public review.
We agree that our statement about the method novelty was confusing in the original version of the manuscript, especially in the sentence from the introduction. We rewrote it to: “Here, we develop a new technique based on biplanar high-speed X-ray videography to quantify the 3D pathlines of intraoral water and combine it with existing methods to track food and quantify 3D skeletal motions.” This should clearly separate the new contribution from the existing methods and make it clear that we see the tracking of water as a separate method in addition to the tracking of food. The latter has indeed been done previously in many 2D x-ray studies, and in more recent 3D biplanar X-ray studies. The revised paragraph in the discussion now reverts back to the x-ray particle tracking protocols that have been used in industrial settings (reference Drake et al. 2011).
-
Evaluation Summary:
How do fish suck food underwater? Using new artificial food particles that are radio opaque and naturally buoyant, Provini et al. imaged the roller-coaster ride that food particles make being sucked-in from outside to inside the fish, using 3D stereo high-speed fluoroscopy. The recordings show fish to have an intriguing ability to generate flows that center the food particles as they enter the buccal cavity that carries them from the outside to the center of the digestive tract. Remarkably, the flow patterns in the mouth that accomplish this seem to differ between the two species of fish studied, although samples sizes are small at present. These new insights will interest biologists working on suction feeding mechanisms ranging from millimeter-sized carnivorous water plants, tadpoles and fish larvae, to large fish …
Evaluation Summary:
How do fish suck food underwater? Using new artificial food particles that are radio opaque and naturally buoyant, Provini et al. imaged the roller-coaster ride that food particles make being sucked-in from outside to inside the fish, using 3D stereo high-speed fluoroscopy. The recordings show fish to have an intriguing ability to generate flows that center the food particles as they enter the buccal cavity that carries them from the outside to the center of the digestive tract. Remarkably, the flow patterns in the mouth that accomplish this seem to differ between the two species of fish studied, although samples sizes are small at present. These new insights will interest biologists working on suction feeding mechanisms ranging from millimeter-sized carnivorous water plants, tadpoles and fish larvae, to large fish and marine mammals, and even gigantic whales. Bioinspired engineers designing rapid underwater suction apparatuses may benefit from harnessing the new insights to elegantly center items of interest.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
-
Reviewer #1 (Public Review):
Suction feeding is recognized as a nearly ubiquitous prey capture mode in fishes, and the hydrodynamics of these flows are reasonably understood. Provoni et al. deal with a role that is as important but much less understood, i.e. the role of these flows in intra-oral prey transport. Specifically, they ask how the flows within the buccal cavity can help transport the prey into the mouth. The major obstacle to understand these flows is that they are internal, so it was difficult to quantify them.
Here, the authors developed and used a technique that enabled tracking of tracer particles that are smaller and less dense than the prey, thereby improving our ability to quantify the flows. They show that the suction flows can be directed towards the esophagus at least in one of the species they used, and that …
Reviewer #1 (Public Review):
Suction feeding is recognized as a nearly ubiquitous prey capture mode in fishes, and the hydrodynamics of these flows are reasonably understood. Provoni et al. deal with a role that is as important but much less understood, i.e. the role of these flows in intra-oral prey transport. Specifically, they ask how the flows within the buccal cavity can help transport the prey into the mouth. The major obstacle to understand these flows is that they are internal, so it was difficult to quantify them.
Here, the authors developed and used a technique that enabled tracking of tracer particles that are smaller and less dense than the prey, thereby improving our ability to quantify the flows. They show that the suction flows can be directed towards the esophagus at least in one of the species they used, and that repeated bidirectional flows can be used to redirect particles trapped at the branchial basket towards the esophagus. In doing so, they highlight the role of the suction flows in transport of food, providing a possible explanation to the ubiquity of suction flows even among fish that don't rely on the external flows to capture their prey.
Quantifying internal flows is a demanding task, and the paper presents new and exciting data. As is typical to new techniques, there are important limitations to its current use. The tracers are larger than those used for particle imaging velocimetry, and are heavier than the water. Therefore, they don't track the water precisely. It is difficult to predict the error generated due to this limitation, because it depends on the velocity gradients in the flow (for example accelerations). Additionally, the number of tracers is limited, so they provide a partial representation of the flows within the mouth. It stands to reason that particles drawn from different locations will have different trajectories, however this is not quantitatively analyzed.
Particle tracking can lend itself to a quantitative analysis of the transport flows, but unfortunately the paper does not take full advantage of these capacities. The intake flow patterns are qualitatively described, and a quantitative estimate of the volume of water that passes near the esophagus are examples for such potential. Other important parameters such as efficiency can be potentially derived directly.
The most important message of the results presented is that the flow of water inside the mouth has a functional role in moving the prey towards the esophagus, and that it can differ between species. These results teach us that the suction flows are important not only to prey capture but also to prey transport.
-
Reviewer #2 (Public Review):
This is a fascinating study that adds great resolution to the mechanisms of water flow in the mouth of fish during suction feeding. Using high-speed x-ray video (XROMM) to track food items and particles in the water, the authors show convincingly that fish have an intriguing ability to generate flows that center the food at the esophagus, and that intraoral flow differs between species. The video is impressive, showing all the particles flow into the mouth, and separation to direct food to the gullet and water to the outflow exit (gill arches).
The methods of XROMM and particle tracking are quite well known – there is nothing new in either approach, nor in combining them to track the prey item. However, the authors created a new kind of marker to enable tracking water flow patterns; a bead surrounded by …
Reviewer #2 (Public Review):
This is a fascinating study that adds great resolution to the mechanisms of water flow in the mouth of fish during suction feeding. Using high-speed x-ray video (XROMM) to track food items and particles in the water, the authors show convincingly that fish have an intriguing ability to generate flows that center the food at the esophagus, and that intraoral flow differs between species. The video is impressive, showing all the particles flow into the mouth, and separation to direct food to the gullet and water to the outflow exit (gill arches).
The methods of XROMM and particle tracking are quite well known – there is nothing new in either approach, nor in combining them to track the prey item. However, the authors created a new kind of marker to enable tracking water flow patterns; a bead surrounded by foam, to create neutral buoyancy, that worked really well. Overall a fascinating study that adds to our understanding of suction feeding in fish.
-
