In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish
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,...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/73621 |
| _version_ | 1828382939312816128 |
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| author | Pauline Provini Alexandre Brunet Andréa Filippo Sam Van Wassenbergh |
| author_facet | Pauline Provini Alexandre Brunet Andréa Filippo Sam Van Wassenbergh |
| author_sort | Pauline Provini |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-10T04:41:10Z |
| format | Article |
| id | doaj.art-a652db7678d348699bf52e6fc6ce7e0d |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:41:10Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-a652db7678d348699bf52e6fc6ce7e0d2022-12-22T02:01:53ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.73621In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fishPauline Provini0https://orcid.org/0000-0002-9374-1291Alexandre Brunet1Andréa Filippo2Sam Van Wassenbergh3https://orcid.org/0000-0001-5746-4621Département Adaptations du Vivant, Paris, France; Université de Paris, INSERM U1284, Center for Research and Interdisciplinarity (CRI), Paris, FranceDépartement Adaptations du Vivant, Paris, FranceDépartement Adaptations du Vivant, Paris, FranceDépartement Adaptations du Vivant, Paris, France; Department of Biology, University of Antwerp, Universiteitsplein 1, Antwerp, BelgiumVirtually 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.https://elifesciences.org/articles/73621Cyprinus carpioOreochromis niloticusfish |
| spellingShingle | Pauline Provini Alexandre Brunet Andréa Filippo Sam Van Wassenbergh In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish eLife Cyprinus carpio Oreochromis niloticus fish |
| title | In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| title_full | In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| title_fullStr | In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| title_full_unstemmed | In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| title_short | In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| title_sort | in vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish |
| topic | Cyprinus carpio Oreochromis niloticus fish |
| url | https://elifesciences.org/articles/73621 |
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