In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish

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 intra-oral water flows 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 patterns of intra-oral water flows 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.

Data availability

All data analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for all figures in Data file S1.

Article and author information

Author details

  1. Pauline Provini

    Département Adaptations du Vivant, UMR 7179 CNRS, MNHN, Paris, France
    For correspondence
    pauline.provini@cri-paris.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9374-1291
  2. Alexandre Brunet

    Département Adaptations du Vivant, UMR 7179 CNRS, MNHN, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Andréa Filippo

    Département Adaptations du Vivant, UMR 7179 CNRS, MNHN, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Sam Van Wassenbergh

    Département Adaptations du Vivant, UMR 7179 CNRS, MNHN, Paris, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-16-ACHN-0006)

  • Sam Van Wassenbergh

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the European recommendations of animal experimentation. All of the animals were handled according to approved institutional animal care and were ethically approved by the University of Antwerp (ECD-2017-22). All surgery was performed under Ethyl 3-aminobenzoate methanesulfonate anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. David Lentink, University of Groningen, Netherlands

Publication history

  1. Received: September 5, 2021
  2. Preprint posted: September 20, 2021 (view preprint)
  3. Accepted: February 21, 2022
  4. Accepted Manuscript published: February 22, 2022 (version 1)
  5. Version of Record published: March 9, 2022 (version 2)

Copyright

© 2022, Provini et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Pauline Provini
  2. Alexandre Brunet
  3. Andréa Filippo
  4. Sam Van Wassenbergh
(2022)
In vivo intraoral waterflow quantification reveals hidden mechanisms of suction feeding in fish
eLife 11:e73621.
https://doi.org/10.7554/eLife.73621
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