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First published online December 2, 2005
Journal of Experimental Biology 208, 4627-4639 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01919

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A test of mouth-opening and hyoid-depression mechanisms during prey capture in a catfish using high-speed cineradiography

Sam Van Wassenbergh^1,*, Anthony Herrel¹, Dominique Adriaens² and Peter Aerts¹

¹ Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610, Antwerpen, Belgium
² Evolutionary Morphology of Vertebrates, Ghent University, K. L. Ledeganckstraat 35, B-9000, Gent, Belgium

View larger version (36K): [in a new window]   Fig. 1. Schematic representation of the four potential mouth-opening mechanisms (A–D) in Clarias gariepinus. The functional elements of the cranial system are represented by different colours: lower jaw, red; hyoid, green; suspensorium, yellow; operculum, blue; cleithrum, yellow and neurocranium, grey. Dark and light colours represent elements that are involved and not involved, respectively, in a particular mechanism. Broken lines correspond to positions of cranial elements and four-bar chains after activity of the mechanisms. More detailed representations of the four-bar systems are given on the right, in which the fixed link is represented by short perpendicular lines. l-an-ch, ligamentum angulo-cerotohyale; l-an-iop, ligamentum angulo-interoperculare; m-l-op, musculus levator operculi; m-pr-h, musculus protractor hyoidei; o-iop, os interoperculare.

View larger version (18K): [in a new window]   Fig. 2. Schematic representation of the two potential hyoid-depression mechanisms (A,B) in Clarias gariepinus. Colours and symbols correspond to those in Fig. 1. l-puh-hh, ligamentum parurohyalo-hypohyale; m-epax, epaxial muscles; m-hypax, hypaxial muscles; m-sh, musculus sternohyoideus; o-puh, os parurohyale.

View larger version (137K): [in a new window]   Fig. 3. Position of the inserted radio-opaque markers (coloured circles) and additional landmarks (white circles) digitized to define the fish-bound frame of reference (white broken lines) imposed on a lateral (A) and dorsoventral (B) X-ray image of Clarias gariepinus (70.2 mm cranial length). Contours of the lower jaw (red), hyoid bars (green), cleithrum (orange), suspensorium (yellow) and operculum (blue) are shown. The markers are: (1) the upper jaw tip, (2–4) landmarks on the roof of the buccal cavity, (5) anterior of the neurocranium, close to the occipital process, (6) lower jaw tip, (7,8) more caudal points on the left and right lower jaw, (9) rostral tip of the hyoid, (10,11) approximate middle along left and right hyoids, near the origin of the protractor hyoidei muscles, (12) tip of the cleithrum, (13,14) caudal points on the left and right side of the cleithrum, near the base of the pectoral fins, (15) suspensorium and (16) operculum. Landmark (1) was taken as origin (0,0) and the X-axis is parallel to the least-squares linear regression through points (1–4).

View larger version (55K): [in a new window]   Fig. 4. Selected X-ray video frames from a representative prey capture sequence (0–240 ms) of a Clarias gariepinus individual (70.2 mm cranial length, Catfish A) equipped with radio-opaque markers during feeding on an attached shrimp.

View larger version (25K): [in a new window]   Fig. 5. Kinematic profiles of the two mouth-opening types observed in C. gariepinus, as illustrated for one individual (catfish A). Values are means ± S.E.M. (N=15 for Type 1; N=5 for Type 2). The grey bar indicates the period of the additional acceleration that can be observed during `type 1' mouth opening. See text for further information.

View larger version (31K): [in a new window]   Fig. 6. Mean mouth-opening (0–100%) and mouth-closing (100–200%) profiles with the calculated four-bar model output for each of the mouth opening mechanisms during `type 1' mouth openings (A–C, top), together with length of the protractor hyoidei (m-pr-h; A–C, bottom). Separate graphs are shown for each individual: A (N=15), B (N=12) and C (N=13). Grey bars indicate the time during which the protractor hyoidei shorten. The shaded areas accompanying each curve indicate S.E.M. The broken, green curves give average four-bar model output of mechanism 1C with the protractor hyoidei at minimum length (upper curve) and at maximum length (lower curve) as coupler. Colour codes are indicated in the key above the figure. Mech. 1A,1B,1C, see Fig. 1.

View larger version (29K): [in a new window]   Fig. 7. Mean mouth opening (0–100%) and closing (100–200%) profiles with the calculated four-bar model output for each of the mouth opening mechanism during `type 2' mouth openings (A–C, top), together with length of the protractor hyoidei (m-pr-h; A–C, bottom). Separate graphs are shown for each individual: A (N=5), B (N=8) and C (N=7). Grey bars indicate the time during which the protractor hyoidei shorten. The shaded areas accompanying each curve indicate S.E.M. The broken, green curves give average four-bar model output of mechanism 1C with the protractor hyoidei at minimum length (upper curve) and at maximum length (lower curve) as coupler. Colour codes are indicated in the key above the figure. Mech. 1A,1B,1C, see Fig. 1.

View larger version (26K): [in a new window]   Fig. 8. Mean hyoid depression (0%–100%) and elevation (100%–200%) profiles with the calculated four-bar model output for hyoid-depression mechanism 2A (A–C, top), together with length of the sternohyoideus muscle (m-sh; A–C, bottom). Separate graphs are shown for each individual (N=20). The shaded areas accompanying each curve indicate S.E.M. Note that these S.E.M. values are larger in case the radio-opaque marker is absent at the tip of the cleithrum (B,C). The lower and upper broken, grey lines represent the output of the four-bar model with, respectively, a fully elongated sternohyoideus muscle and the sternohyoideus at minimum length. The latter curve is partly not displayed in B when there were no analytical four-bar solutions in more than half of the cases. Grey bars indicate the period during which the sternohyoideus shortens. Colour codes are indicated in the key above the figure. Mech. 2A, see Fig. 2.

View larger version (16K): [in a new window]   Fig. 9. A representative prey capture sequence of C. gariepinus showing a reconstruction of four-bar kinematics of mechanism 1B (Fig. 1B) during mouth opening (A) and mouth closing (B). Both the observed hyoid angle (green line) and lower jaw angle (red line) were used as input, whereas the length of the coupler link (i.e. the angulo–ceratohyal ligament; thick grey line) was adjusted to fit the observed hyoid and lower jaw kinematics. Note that the angulo–ceratohyal ligament elongates during mouth opening, but is stretched again during mouth closure, during which it helps to elevate the hyoid.