Solid-liquid filtration is a ubiquitous process found in industrial and biological systems. Although implementations vary widely, almost all filtration systems are based on a small set of fundamental separation mechanisms, including sieve, cross-flow, hydrosol, and cyclonic separation. Anatomical studies showed that manta rays have a highly specialized filter-feeding apparatus that does not resemble previously described filtration systems. We examined the fluid flow around the manta filter-feeding apparatus using a combination of physical modeling and computational fluid dynamics. Our results indicate that manta rays use a unique solid-fluid separation mechanism in which direct interception of particles with wing-like structures causes particles to “ricochet” away from the filter pores. This filtration mechanism separates particles smaller than the pore size, allows high flow rates, and resists clogging.

Manta rays are large elasmobranchs that feed by swimming with open mouths, capturing small zooplankton (51 to 100 μm), microcrustaceans (101 to 500 μm), and mesoplankton (>500 μm) while expelling seawater through the gill slits ( 11 , 18 ). The filtering apparatus in these animals is a highly modified gill raker, comprising long, parallel arrays of leaf-like filter lobes ( 11 , 18 – 20 ). Water moves unidirectionally through the buccal cavity, over the filters, and is expelled out the filter pores to the parabranchial chamber. The orientation of the filter lobes within the cavity suggests that water impinges on the filters in both forward (wing-like posterior filters) and reversed (spoiler-like anterior filters) directions ( Fig. 1 ). Despite an understanding of the anatomy, the separation mechanism used by this filtering apparatus is not clear. In contrast to what would be expected for sieve, cross-flow, hydrosol, and cyclonic separation mechanisms, these animals capture nearly neutrally buoyant particles smaller than the pore size using nonsticky filter elements without clogging ( 20 ).

A large diversity of aquatic animals feed by filtering plankton and other food particles out of the water. It had long been thought that many teleost fish species capture prey by sieving, passing plankton-laden water through elongate gill rakers that protrude from the gill arches into the pharynx. However, gut content analysis in several teleost fish species demonstrates that fishes routinely capture plankton smaller than the openings between the gill rakers, indicating that this process is more complex than simple sieving ( 14 , 15 ). Several recent studies have examined flow in the buccal cavity and suggest that cross-flow filtration plays an important role in filter-feeding in teleost fishes ( 5 , 15 ) and that separated vortices may generate additional clearing action that further reduces clogging ( 16 , 17 ). In addition, many animals are known to feed using hydrosol-based mechanisms, including bryozoans, crinoids, and sponges ( 10 ). It would be surprising for large fishes to rely on hydrosol filtration, as this would require large volumes of mucus and produce filter clogging. To our knowledge, cyclonic filtration has not been demonstrated in any organism.

Several fundamental mechanisms for solid-fluid separation have been described in the biological and engineering literature, including sieve ( 1 , 2 ), cross-flow ( 3 – 6 ), hydrosol ( 7 ), and cyclonic separation ( 8 ). Sieve filtration passes a mixture of particles and fluid through a structure with regularly sized pores, causing the particles to be retained while the fluid is drained. Although effective, sieve filters must have pore sizes smaller than the particle size, and they inevitably clog in use ( 2 , 8 , 9 ). Cross-flow filtration is similar to sieving, except that the incoming flow runs parallel rather than perpendicular to the filter. This configuration shears captured particles off the filter’s surface, which reduces but does not eliminate clogging ( 5 , 6 ). Unlike sieve and cross-flow filters, hydrosol and cyclonic filtration do not require regularly sized pores. Hydrosol filtration captures particles using “sticky” structures within the filters, which allow these filters to capture particles smaller than their pore size, although they also invariably become clogged ( 10 , 11 ). Cyclonic filtration uses a high-speed, rotating flow that flings dense solid particles to the periphery while allowing fluid to pass through the center ( 8 , 12 , 13 ). This separation mechanism requires the solid particles to be denser than the fluid but is resistant to clogging ( 12 ) and has been widely used within the bagless vacuum industry ( 12 , 13 ).

RESULTS AND DISCUSSION

To examine how these animals capture plankton, we examined flow over a physical model of the filtering apparatus. A three-dimensional (3D) printed model of an array of filter lobes was manufactured using morphological parameters measured in Manta birostris (Fig. 1, A and B). We positioned this model in an open-ended flow tank that was adjusted to mimic the flow conditions in the buccal cavity of M. birostris (fig. S1A). Since experimental measurements of the flow velocities in the buccal cavity are not available, the freestream and transverse flow velocities were estimated using swimming speeds, the continuity equation, and anatomical data (see Materials and Methods). Neutrally buoyant particles larger than the pore size would be expected to be filtered with 100% efficiency. To test the performance limits of the filter, we examined neutrally buoyant particles (hydrated Artemia sp. cysts; average diameter, 275 μm) that were smaller than the pore size (>99% of the cysts smaller than pore size of 340 μm; fig. S1B) and would pass through the model if it were functioning as a sieve filter. Filtered and unfiltered water was collected and used to calculate filtration efficiency. We found that a large fraction of these particles were also excluded by the filter (wing, 19 ± 5% efficiency; spoiler, 62 ± 5% efficiency; mean ± SEM), and visual inspection revealed no clogging.

These results suggest that the manta filtering apparatus can separate small particles from the fluid, but what is the mechanism behind this effect? To address this question, we placed a 3D-printed physical model of a filter lobe array into a recirculating flow tank, again matching the freestream and transverse flow velocities to estimates for the buccal cavity. Flow around the filter was visualized by injecting dye upstream and imaging the dye pathlines around the filter (Fig. 1, C and D). This approach allowed us to identify the flow structures around the filter lobes, even in cases where small spaces, reflection, and occlusion would complicate quantitative analysis (for example, particle image velocimetry). We found that the flow over the filter lobes is markedly different than expected for a typical sieve filter. In the wing orientation, flow separation occurred behind the leading edge of each filter lobe, resulting in a large, captive vortex within each pore. Filters in the spoiler orientation displayed similar flow patterns, although the direction of the freestream flow was reversed.

To better understand how solid particles interacted with the filtering apparatus, we next introduced neutrally buoyant particles (hydrated Artemia sp. cysts) into the upstream flow and recorded the trajectory of these particles as they passed over the filter (Fig. 1, E and F). For the wing orientation, we observed that particles often directly impacted the leading edge and were then re-entrained within the freestream flow. Similarly, we observed increases in the vertical velocity at positions corresponding to the leading edge of the filter lobes. In the spoiler orientation, particles passing over the filter appeared to glide over the trailing edge of each filter lobe before being re-entrained within the flow, and there were similar increases in the vertical velocity at corresponding locations.

What physical forces cause the particles to be repelled away from the filter while allowing fluid to pass through? To address this question, we constructed a computational fluid dynamics (CFD) model of the flow over an array of filter lobes (Fig. 2A). As with the physical models, the model geometry was based on morphological measurements in M. birostris, and the freestream and transverse flow velocities mimicked those in the buccal cavity. To visualize the flow fields, we calculated the fluid streamlines that pass through a pore near the center of the array. For the wing orientation, these streamlines indicate that water glides above the lobe array, forms a thin boundary layer on the upstream surface of the lobe, is swept around a captive vortex within the pore, and is then washed into the filtrate flow. The streamlines for the spoiler orientation are surprisingly similar, except that the streamlines exhibit more pronounced curvature as they pass around the captive vortex. These flow fields closely mirror the results from our dye visualization experiments. In addition, the computed hydrodynamic resistance was very low for both the wing and spoiler orientations (wing, 1161 Pa s m−1; spoiler, 1673 Pa s m−1), consistent with previous experimental measurements (11). Since the energetic cost of filtration is proportional to the hydrodynamic resistance for a fixed flow rate, these low hydrodynamic resistance values may have an important role in limiting energetic expenditure and achieving energy balance in this group of animals.

Fig. 2 Computational modeling indicates that solid particles ricochet off manta ray filter lobes. (A) Flow field around the M. birostris filtering apparatus in wing (top) and spoiler (bottom) configuration, predicted using CFD model (streamlines in white; background indicates the velocity magnitude). (B) Calculated trajectories of fluid (blue) and solid particles (center of mass, red; diameter, 350 μm; neutrally buoyant) as they pass over the filtering apparatus. The outline of a representative particle (dark red) shows the size of the particles relative to the filtering apparatus. Although they start from the same position, fluid passes through the filter pore, while solid particles are excluded. (C) Predicted filtration efficiency of the apparatus as a function of solid particle diameter and density (in kg/m3), with the pore size indicated. Sizes of plankton indicated on the background. Small zooplankton (51 to 100 μm; dark gray), microcrustaceans (101 to 500 μm; medium gray), and large zooplankton (>501 μm; light gray).

To understand how these flow patterns produce solid-fluid separation, we next constructed a computational model to simulate the motion of particles carried by the flow (Fig. 2B). Spherical particles were introduced into the flow upstream of the filter array, with initial positions distributed across the fluid streamlines that passed through a filter pore near the center of the array. Since the solid particles were released along fluid streamlines, deviation of a solid particle from the corresponding streamline indicates solid-fluid separation and solid particles that do not pass through the pore represent filtration events.

For the wing orientation, simulated solid particles initially follow fluid streamlines and glide over the top of the filter array. However, as the fluid approaches a filter element, streamlines pass very near to the leading edge of the filter lobe before being diverted into the filter pore. Since they have finite size, solid particles cannot follow this path and encounter the leading edge of the filter lobe by direct interception. Instead of sticking as in classic hydrosol filtration, contact forces cause the particles to “ricochet” away from the filter pore and back into the faster-moving freestream flow. This process repeats at the next filter lobe and causes the particles to be repeatedly excluded from the filtrate. These conclusions and the simulated particle trajectories are in agreement with the results of our physical modeling experiments (Fig. 1, E and F, versus Fig. 2B). Contact forces also appear to play a key role in solid-fluid separation for filters in the spoiler orientation. In this case, we found that simulated solid particles initially followed streamlines as they passed over the filter array. However, the fluid streamlines then passed very close to the trailing edge of the preceding lobe. As for the wing orientation filters, solid particles with finite size cannot follow these streamlines and contact forces cause the particles to ricochet back into the faster freestream flow. This process has parallels to direct interception hydrosol filtration in which a particle following a streamline collides with a sticky surface and is captured (1). However, here, the particle recoils elastically from the surface and moves into streamlines that pass over the filter pore, resulting in concentration of particles in the water above the filter.

We next calculated the filtration efficiency for particles with a range of sizes and densities. We found that filtration efficiency increased markedly when the particle size exceeded ~200 μm, which is notably smaller than the filter pore size of 340 μm (fig. S2B). In contrast, changes in particle density had relatively little effect on filtration efficiency, within a biologically realistic range of densities. This size selectivity agrees with our physical modeling and with estimates from wild manta rays as well (11, 18). Insensitivity of the filtration process to particle density is consistent with the ricochet solid-fluid separation mechanism, which results from contact forces that are not directly affected by the specific density of the solid particle. It is possible that the complex shapes and escape responses of zooplankton would also affect capture dynamics (21, 22). Although these effects are difficult to quantitatively model with the data available, the shear stress at the filter lobes might be expected to elicit escapes responses away from the filter, which could also enhance the observed filtration effects.

Since the freestream flow velocity appeared to have a major role in establishing the flow fields that drive the solid particles to contact the filter lobes (fig. S3, A and D), we next asked how the freestream flow velocity affects filtration efficiency. The CFD model was solved for a range of freestream velocities (0.05 to 0.7 m/s), while the pressure across the filter was held constant, and the filtration efficiency was calculated for 300-μm neutrally buoyant particles (fig. S3, E and F). We found that filtration efficiency increased sharply when freestream velocity exceeded 0.300 m/s, which is about half of the estimated velocity. This dependence on the freestream flow velocity is consistent with the proposed mechanism and also suggests that the mechanism operates effectively over a large range of freestream flow velocities.

In classic direct interception filtration, capture efficiency increases with Reynolds number (Re) as a result of streamline compression (23, 24). To determine whether there is a corresponding effect in mobulid filters, the CFD model was solved for a range of Re values, and the filtration efficiency was calculated for neutrally buoyant particles (fig. S3, G and H). To preserve similitude, Re was varied by changing fluid viscosity while holding freestream and transverse velocities constant. For both spoiler and wing configurations, the predicted filtration efficiency was zero for low Re, increased with Re, and reached 100% for Re greater than ~900. This threshold is just below the value estimated for freely swimming M. birostris (Re = 1075), which may suggest that Re is maintained at a value large enough to produce filtration but small enough to limit turbulence. These results also indicate that smaller particles cannot be captured by simply scaling down the filter morphology while holding fluid properties and flow velocities constant, since this is equivalent to decreasing Re and results in a decrease in filtration efficiency. However, smaller particles would be expected to be filtered if the morphology was scaled down while fluid velocities were increased to hold Re constant.

We also examined how qualitative changes in the filter morphology might affect filtration. Micro–computed tomography (μCT) was used to reconstruct the 3D morphology of the filtering apparatus of Mobula tarapacana, which have a similar filtering apparatus to M. birostris except with pore sizes approximately four times larger (Fig. 3A and fig. S4). As above, a computational model was used to predict the flow field and plankton trajectories around the filtering apparatus using freestream and transverse velocities estimated for M. tarapacana. Although the pore was 1100 μm wide, filtration efficiency rapidly increased for particles larger than ~250 μm. Similar to M. birostris, simulated plankton particles were excluded by the filter following contact with the tips of the filter lobes. These results indicate that M. tarapacana and M. birostris feed using a similar solid-fluid separation mechanism and that this mechanism can effectively filter particles that are much smaller than the pore size (Fig. 3B). Compared to M. birostris, the filtering apparatus of M. tarapacana was predicted to operate with approximately six times smaller transverse velocity (~10 mm/s versus ~57 mm/s) and require approximately seven times smaller pressure head (wing, 11 Pa versus 56 Pa; spoiler, 11 Pa versus 100 Pa) but filter plankton particles of similar size (Fig. 3C). These differences may reflect specialization of the filtering apparatus for different foraging strategies. Since M. tarapacana is predicted to have a lower flow rate and pressure head, it would be expected to have reduced plankton consumption but would also be expected to have decreased drag and energetic expenditure. A detailed comparison would require more information on feeding behaviors and the plankton size distribution where the fishes are actively feeding but would be a very interesting area for future studies.

Fig. 3 Morphology of filtering apparatus determines filtration properties. (A) M. tarapacana filter (top) and a μCT reconstruction of a single row of filter lobes (bottom) (photo credit: E.W.M.P.-T., CSUF). (B) Calculated trajectories of fluid (blue) and solid particles (center of mass, red; diameter, 350 μm; neutrally buoyant) as they pass over the filtering apparatus. The outline of a representative particle (dark red) shows the size of the particles relative to the filtering apparatus. (C) Predicted filtration efficiency of the apparatus as a function of solid particle diameter and density (in kg/m3), with the pore size indicated. Sizes of plankton indicated on background. Small zooplankton (51 to 100 μm; dark gray), microcrustaceans (101 to 500 μm; medium gray), and large zooplankton (>501 μm; light gray).

Our results suggest that the manta ray filtering apparatus operates through a unique solid-fluid separation mechanism, which we have termed ricochet separation. This solid-fluid separation mechanism may have interesting industrial applications, since it operates at high flow rates, effectively filters neutrally buoyant particles, and resists clogging. Captured particles are concentrated above the filter rather than forming a cake over the filter, which may obviate the need for secondary cleaning mechanisms that are often costly and time consuming (8, 25). In addition to the engineering applications, mobulid rays are increasingly being targeted by illegal commercial and artisanal fisheries (26–28), and an improved understanding of the physiology of filter feeding may be useful for predicting the habitat usage of mobulid rays and implementing appropriate protective measures.