Fish Feeding

Biomechanics of jaw protrusion in common carp

N.J. Gidmark1*, K.L. Staab2, E.L. Brainerd1, and L.P. Hernandez2

  1. Brown University, Providence, RI, USA
  2. The George Washington University, Washington D.C., USA

Published article | Abstract

In this study we are using X-ray Reconstrucion of Moving Morphology (XROMM) to examine the movements of several oral jaw bones and understand the mechanics of jaw protrusion in common carp, Cyprinus carpio.

Cypriniform fishes (commonly known as minnows, carps, goldfish, koi and loaches) are capable of impressive protrusion of the oral jaws (Figure 1). This protrusion can be observed in conjunction with or separate from opening of the mouth, likely resulting in nuanced control of water flows within the oral and pharyngeal cavities (Movie 1). This control is pivotal for the bottom-feeding lifestyle of common carp. One morphological oddity that can be seen in common carp (and in all cypriniform fishes except three species, which have secondarily lost it) is the presence of the kinethmoid, a highly mobile midline bone (Figure 2) located in a ligamentous meshwork supported by upper jaw bones and the neurocranium. Because of its location in ligaments and occluded by other bones, even anatomical preparations aimed at demonstrating bone may not show it clearly (Figure 3). Because of these limitations, previous in-vivo studies have been unable to explicitly examine its movements or the mechanics of how the upper jaws are protruded in kinethmoid-bearing species. We used marker-based (Figure 4) XROMM to create precise and accurate animations of 3D oral jaw bones and their motions during jaw protrusion in suction-feeding carp (Movie 3) based on x-ray videos (Movie 2). We used anatomical axes to track specific anatomically relevant degrees of freedom in these bones during both open-mouth (Figure 5) and closed-mouth (Figure 6) protrusion events. Kinematic curves for the ventral translation of the maxilla, premaxillary protrusion, and lower jaw rotation are all three highly correlated (based on a cross correlation analysis without lag) with kinethmoid rotation in both open-mouthed (Figure 7) and closed-mouth (Figure 8) protrusion events. Since the lower jaw is the only one of those movements that is less pronounced in closed-mouth trials, we hypothesize that muscles attaching to the maxilla (specifically A1beta) drive the maxilla to translate ventrally. We further hypothesize that maxillary translation causes kinethmoid rotation and ultimately premaxillary protrusion. These findings are significant for two reasons. First, we have experimental evidence indicating how this novel mechanism of jaw protrusion functions biomechanically. Second, and possibly most important, we have empirically shown decoupling of upper jaw protrusion from lower jaw abduction. Most fishes that protrude the upper jaw do so by abducting the lower jaw. The decoupling seen in common carp is likely a derivation that allows for precise control of water flows within the mouth and thus great dexterity in sorting food particles from the substrate where these fishes feed.

Pictures

Common carp have highly kinetic skulls which allow them to protrude their upper jaws. This may aid in suction feeding performance and food-sorting within the oral cavity. In addition to typical fish skull upper jaw bones such as the maxilla and premaxilla, cypriniform fishes develop a novel bone, the kinethmoid. This mobile bone is embedded between the maxillae along the midline of the fish. Even in a stained an cleared preparation, which is specifically designed to demonstrate bone shape, a meshwork of ligaments and other bones makes the kinethmoid difficult to see in-situ. Can you find it here? This medial view of the oral jaw bones in carp demonstrates our marker placement for this study. Neurocranium markers have not been included. Once we have an xromm, we can use anatomically-relevant axis systems to describe the 6 degrees of freedom of each bone relative to other bones. Here, two of the axes of the maxilla are demonstrated for an open-mouthed protrusion. Rotation about the magenta axis shows parasagittal rotation of the maxilla; rotation about the blue axis shows long-axis rotation of the maxilla; translation along the blue axis shows ventral translation of the maxilla. In this frame, the same axis system as Photo 5 is shown, only now the animal is performing a closed-mouth protrusion. Movement patterns of protrusion, ventral translation of the maxilla, lower jaw rotation, and parasagittal rotation of the maxilla are very highly correlated with the kinethmoid's movement pattern (y-axis values close to 1), whereas other maxillary degrees of freedom are not correlated during open mouth protrusion. During closed mouth protrusion, ventral translation is the only maxillary movement pattern that is correlated significantly with kinethmoid rotation.

Movies

Fish Feeding: Light video Fish Feeding: X-ray video Fish Feeding: XROMM animation