How organisms acquire food is largely determined by the medium in which they feed (Herrel et al., 2012). Aquatic organisms commonly exploit the dense and viscous properties of water to carry food from a distance, toward and through their mouth, by generating flows of water. These flows typically result from suction created by a powerful expansion of the feeding apparatus, for example, in fishes that suddenly increase the volume of their buccopharyngeal cavity (Alexander, 1969). This action is referred to as "suction feeding".

A wide range of aquatic vertebrates across a large size range employ suction feeding: from larval fishes (Drost et al., 1988) and frog tadpoles (Deban and Olson, 2002) to whales (Werth, 2004), and some carnivorous plant with tiny suction traps (Müller et al., 2020). Because of this impressive diversity in organisms making use of suction feeding, it plays an important role in all major aquatic habitats and feeding niches throughout the water column (Wainwright et al., 2015).

In virtually all fishes, waterflows generated by suction are essential for transporting food inside the buccal cavity (Labarbera, 1984; Potvin and Werth, 2017; Wainwright et al., 2015). During suction feeding, the three-dimensional (3D) waterflow patterns toward the fish’s mouth have been particularly well studied (Day et al., 2007; Nauwelaerts et al., 2008; Skorczewski et al., 2012; van Leeuwen, 1984). Although waterflow patterns external to the mouth depend on the approaching speed of the fish (Kane and Higham, 2014; Muller and Osse, 1984), instantaneous streamline patterns are fairly conserved between species and behaviors (Jacobs and Holzman, 2018): as the 3D streamlines converge toward the gape (Figure 1a, blue arrows), food items that are initially somewhere close to the mouth will curve into the buccal cavity by these extraoral waterflows.

Figure 1

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In contrast to this relatively straightforward and well-resolved mechanism of food capture toward the mouth, food transport mechanisms inside the buccopharyngeal cavity are not as simple (Callan and Sanderson, 2003; Divi et al., 2018; Sanderson et al., 1991; van Meer et al., 2019) and are largely unknown (Day et al., 2015). After passing through the mouth opening (Figure 1a, blue arrows), water streamlines are generally assumed to diverge along with the widening buccopharynx (Figure 1a and b, red arrows; Muller et al., 1985; Provini and Van Wassenbergh, 2018). This implies that, inside the buccal cavity, waterflow tends to be directed toward the gill slits, located at the posteroventral and posterolateral head margins (Figure 1b). Paradoxically, as these flows take a short route to the gill slits, they seem far from optimal to carry food to the entrance of the esophagus, along the midsagittal plane of the buccal cavity.

To date, there is no evidence that the esophagus expands in concert with buccopharyngeal suction generation to directly draw in a significant amount of water together with the food. Therefore, other structures need to be involved in separating food from the waterflows. Ideally, in bony fish, the food that is sucked into the mouth could be intercepted by the pharyngeal jaws located just anterior to the esophageal sphincter (Figure 1). The mobile pharyngeal jaws, while maintaining physical contact with the food, can move it to the esophagus (Liem, 1978; Sibbing et al., 1986). However, given the current hypothesis of diverging streamlines in the expanding buccopharyngeal cavity (Figure 1a and b), food is more likely to end up being sieved by the other branchial arches and their gill rakers, after which a second food transport cycle is needed, encountering the same problem regarding how the food is able to reach the esophagus. Consequently, intraoral hydrodynamics are critical in determining the initial food deposit site after capture and, in turn, the associated anatomical adaptations and behaviors for food transport and handling inside the head.

Alternatively, two other intraoral flow patterns are theoretically possible, which may facilitate interception by the pharyngeal jaws (Figure 1c and d). Computational models of suction-feeding hydrodynamics (Thompson et al., 2018; Van Wassenbergh, 2015) show that flow can separate from the expanding buccopharynx to create a centralized jet of suction flow, along with anterior flow at the borders of the buccal cavity forming vortices (Figure 1c). This pattern, to which we will refer as a "central jet", could carry food closer to the pharyngeal jaws (Figure 1c) compared to the classical hypothesis of "diverging flow" (Figure 1b). Thirdly, as hypothesized for fishes relying on filtration of smaller food particles from the water (Brooks et al., 2018; Sanderson et al., 2001), gill arch and raker structures may cause crossflows, in which the main direction of flow medial to the branchial arches is directed toward the esophagus and only the permeate of the branchial filter basket flows out through the gill slits (Figure 1d).

Despite this critical role during feeding in nearly all fishes, the spatiotemporal pattern of intraoral waterflow has still not been quantified in vivo due to the difficulty in gaining optical access to the buccopharyngeal cavity. This implies a fundamental gap in our knowledge regarding how more than half of all vertebrates feed. Here, we develop a new technique based on biplanar high-speed X-ray videography to simultaneously quantify the 3D path lines of both food and intraoral water, as well as skeletal kinematics. We apply this technique to two distantly related omnivorous suction feeders, carp (Cyprinus carpio) and tilapia (Oreochromis niloticus). These species were chosen from the large diversity of suction feeders because their adult head size is small enough to fit the imaging volume of the biplanar X-ray setup, yet large enough to avoid hindrance from an intake of tracer particles for waterflow inside the buccal cavity using X-rays. We use this data to describe the intraoral waterflow and determine the intraoral mechanisms of aquatic feeding that have remained hidden thus far.

This first application of neutrally buoyant X-ray particle tracking in biological research allowed us to quantify 3D waterflow patterns inside the mouth of a live fish with satisfactory spatial and temporal resolution (time resolution: 750 fps; spatial resolution of the biplanar X-ray device: ± 0.1 mm; Sanctorum et al., 2019). Despite the inevitably low number of tracked particles (<20) compared to common, light-optical techniques using dense suspensions of considerably smaller seeding particles (e.g., particle-tracking velocimetry), we managed to resolve the flow speeds and directions in the vicinity of the food. Compared to previously employed invasive techniques to quantify intraoral flows, such as endoscopy (Callan and Sanderson, 2003; Smith and Sanderson, 2008) or pressure recordings (e.g., Van Leeuwen and Muller, 1982), our noninvasive approach yields a more complete view of the spatial aspects of intraoral suction-feeding dynamics, allowing us to demonstrate the existence of different hydrodynamic mechanisms for food transport.

The new particle-tracking technique we described here (Figure 7a–d) can be easily combined with 3D motion reconstruction protocols for skeletal elements (i.e., X-ray reconstructions of the moving morphology [XROMM]; Brainerd et al., 2010) to link waterflow patterns to skeletal kinematics (Figure 5). The relatively straightforward, inexpensive, yet time-consuming protocol to construct the particles, as proposed in this study (Figure 7a–d), may be further optimized to reduce the variability in density (Figure 7d). That way, particles could be kept in suspension in the water column for longer periods and allow an accurate tracking for a wider range of waterflows, including those involving less strong pressure gradients than during suction feeding. Mold-based manufacturing protocols for metal-cored expanded polystyrene (EPS) spheres, currently available for relatively large particles with a diameter of 8 mm (Drake et al., 2011), could perhaps be miniaturized. In any case, the method of X-ray particle tracking has strong potential to become an indispensable tool for studying form–function relationships and the biomechanics of various functions involving water motions to which we lack optical access.

The main question of our study was how food ends up at the esophagus entrance when the water that carries the food is traveling elsewhere – namely, to the outflow at the gill slits. If water was a pure "carrier" of the food, it would follow our water tracer’s trajectory from the entrance of the buccal cavity to end up in physical contact with the gill rakers (Figure 1). However, both carp and tilapia appeared to be well capable of positioning the food close to the midsagittal streamlines, thereby avoiding the food from becoming laterally deviated and ending up adhering to the branchial basket. Despite the fact that only a small proportion of the water path lines passed close to the pharyngeal jaws (Figure 3), direct interception of the food item by the pharyngeal jaw was common, which avoided the need for subsequent intraoral food-handling actions.

We hypothesize that fish make use of two mechanisms to cause the food to follow a midsagittal trajectory toward the esophagus: (1) developing a "central jet" flow pattern inside the buccal cavity (Figure 1c) and (2) exploiting the food’s inertia and finite size. Our study found support for the first mechanism by showing a centrally concentrated flow with reverse flow developing near the borders of the buccal cavity (Figures 4 and 6, Figure 6—video 1). This central jet (Figure 1c) was previously reported in computational modeling studies (Thompson et al., 2018; Van Wassenbergh, 2015; Figure 6), but was not given any attention thus far. It was thought to be an artifact of not having included a water outflow trough gill slits in 3D models of expanding heads (Figure 6a; Thompson et al., 2018) or a potential artifact of the hydrodynamic simplification in models using steady flow conditions in nonexpanding heads (Figure 6b; Provini and Van Wassenbergh, 2018). However, the current experimental results show that similar central jet patterns can be present in vivo. The computational fluid dynamics (CFD) models indicate that a diverging flow pattern (Figure 1b; Figure 6a at 2.5 ms) gradually transitions into a central jet by narrowing in course of the suction event. Since a narrowing of the main suction stream will increase the chance of food interception close to the esophagus entrance by the pharyngeal jaws (Figure 1b and c), this will enhance suction efficiency. Further research will be required to unravel why the central jet was more prominent in tilapia (Figure 4b) compared to carp (Figure 4a), which should be related to differences in mouth shape, buccal cavity shape, or expansion kinematics.

Figure 6 with 1 supplement see all

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Secondly, the path curvature from a dorsoventral viewing perspective was significantly higher for the water tracers compared to the food tracers (Figure 4), indicating that inertial effects are at play. For the large prey that fill the bulk of the buccopharyngeal cavity, such inertial effects would be logical and intuitive. However, our data suggest that these mechanisms, in essence a type of filtration, are also present and effective for a relatively small pellet. A similar mechanism is hypothesized to underlie the process of crossflow filtration in filter feeders in the flows that pass close to the branchial arches (Sanderson et al., 2016; Sanderson et al., 1991), but here we show that such an inertial separation mechanism is present at the full scale of the buccopharyngeal cavity. The effect of the size, shape, and density of food on its trajectory in a flow field, as shown in our work (Figure 3, Figure 3—figure supplement 1), remains to be further quantified to fully understand the constraints of the observed filtration mechanism during the initial phase of food intake. Although flow patterns matching those of a branchial crossflow could not be identified (Figure 1d), the fish may not have employed this technique because the food type that was offered may not require it to be filtered in such a way.

As shown in previous work (Olsen et al., 2019; Sibbing, 1982; Sibbing et al., 1986; van Meer et al., 2019; Weller et al., 2020), the feeding process is far from finished after the initial capture in the buccopharyngeal cavity, especially in omnivorous species that perform food sorting and processing. We observed regular and periodical back-and-forth motions of the water tracers after this intake, which moved the food back and forth inside the buccal cavity, with the food finally ending up near the entrance of the esophagus (Figure 2). Rfs, directed toward the anterior part of the buccal cavity and previously referred as ‘back-wash’ (Sibbing et al., 1986), were previously observed in carp (Callan and Sanderson, 2003) and tilapia (Smith and Sanderson, 2008). In carp, anterior movement of the food has been observed using X-ray videos, after which a muscular structure packed with taste buds – the palatal organ – is hypothesized to locally bulge to clamp onto edible particles between the pharyngeal roof and floor, while small waste particles are flushed through the branchial slits (Sibbing, 1988; Sibbing et al., 1986). The anteromedial direction of the flows observed in this study during the rf phase (Figure 3b) seems ideal to bring food particles from both the gill rakers and from the pharyngeal region toward the palatal organ. Overall, these back-and-forth flows are clearly important in the process of sorting food items from the nonedible particles present in the ingested water, and they potentially also prevent the gill slits from clogging. Rfs most likely involve the gill slit functioning as a flow inlet, a function that has rarely been studied (Van Wassenbergh et al., 2016).

Our data provide the first empirical evidence of bidirectional waterflows being synchronized with motions of the upper and lower jaws, hyoid, and opercula to create anterior-to-posterior waves during bfs and posterior-to-anterior waves during rfs. The anterior-to-posterior wave of head expansion and compression is already well known in fish (Gibb and Ferry-Graham, 2005; Lauder, 1985; Muller and Osse, 1984; Van Wassenbergh et al., 2016). This is interpreted as a mechanism to both ingest and dynamically accommodate a volume of water as it moves anteroposteriorly through the buccal cavity. For both species studied, this classical anterior-to-posterior wave was also observed during the consecutive periodic bf motions. Yet, the associated waterflow was not purely anterior-to-posteriorly directed: the water was also guided toward the ventral part of the buccal cavity (Figure 3) by the hyoid depression, and it deviated toward the gill covers (Figure 4) via the abduction of the opercula (Figure 5). During the backward motions of the water, we never observed any particles entering the digestive tract, thus consolidating our hypothesis that no water enters inside the esophagus. A wave in the opposite direction was synchronized with the rfs, as hypothesized earlier (Sibbing et al., 1986; Van Wassenbergh et al., 2016). The stereotypical bf and rf alternations eventually lead the food to the centerline of the buccal cavity and closer to the pharyngeal jaws, where it will be actively transported toward the digestive tract (Sibbing, 1982).

In conclusion, our study highlights the biomechanical complexity of the processes occurring inside the mouth cavity during aquatic feeding in fishes. We showed how high-velocity suction flow patterns during the initial food intake phase can have an effect on the food’s initial deposit site, and how centralized suction streams may help to direct food toward the esophagus. The omnivorous species studied here during benthic feeding followed this phase by repeated, hydrodynamically driven repositionings as part of their food sorting and tasting abilities. Future research using our X-ray particle-tracking technique could further reveal how these processes, and their intraoral hydrodynamic patterns, may vary between feeding modes (e.g., ram-feeders ingesting larger volumes of water), between animals with varying head morphology and size, etc. Such studies would further advance our currently limited insight into the optically invisible processes of aquatic feeding in vertebrates.

All data analysed during this study are included in the manuscript and supporting files.

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Author details

1. Pauline Provini

   1. Département Adaptations du Vivant, Paris, France
   2. Université de Paris, INSERM U1284, Center for Research and Interdisciplinarity (CRI), Paris, France

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Visualization, Writing - original draft, Writing - review and editing

   For correspondence

   pauline.provini@cri-paris.org

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9374-1291

2. Alexandre Brunet

   Département Adaptations du Vivant, Paris, France

   Contribution

   Formal analysis, Writing - review and editing

   Competing interests

   No competing interests declared

3. Andréa Filippo

   Département Adaptations du Vivant, Paris, France

   Contribution

   Formal analysis, Writing - review and editing

   Competing interests

   No competing interests declared

4. Sam Van Wassenbergh

   1. Département Adaptations du Vivant, Paris, France
   2. Department of Biology, University of Antwerp, Universiteitsplein 1, Antwerp, Belgium

   Contribution

   Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5746-4621

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