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

Placoderms are a diverse group of armoured fishes that dominated the aquatic ecosystems of the Devonian Period, 415–360 million years ago. The bladed jaws of predators such as Dunkleosteus suggest that these animals were the first vertebrates to use rapid mouth opening and a powerful bite to capture and fragment evasive prey items prior to ingestion. Here, we develop a biomechanical model of force and motion during feeding in Dunkleosteus terrelli that reveals a highly kinetic skull driven by a unique four-bar linkage mechanism. The linkage system has a high-speed transmission for jaw opening, producing a rapid expansion phase similar to modern fishes that use suction during prey capture. Jaw closing muscles power an extraordinarily strong bite, with an estimated maximal bite force of over 4400 N at the jaw tip and more than 5300 N at the rear dental plates, for a large individual (6 m in total length). This bite force capability is the greatest of all living or fossil fishes and is among the most powerful bites in animals.

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Variation in the feeding kinematics of mole salamanders (Ambystomatidae: Ambystoma)

Canadian Journal of Zoology ◽

10.1139/z95-039 ◽

1995 ◽

Vol 73 (2) ◽

pp. 353-366 ◽

Cited By ~ 8

Author(s):

John T. Beneski Jr. ◽

John H. Larsen Jr. ◽

Brian T. Miller

Keyword(s):

Feeding Behavior ◽

High Speed ◽

Prey Capture ◽

Mouth Opening ◽

General Increase ◽

Feeding Kinematics ◽

High Speed Cinematography ◽

Mode A ◽

General Reduction

High-speed cinematography was used to investigate the prey-capture kinematics of six species of mole salamanders (Ambystomatidae). We compared the feeding behavior of the subgenus Ambystoma (A. californiense and A. macrodactylum) with that of the subgenus Linguaelapsus (A. mabeei, A. texanum, A. annulatum, and A. cingulatum). Prey capture by all six species is characterized by a 3-part gape cycle (a period of rapid mouth opening prior to extraoral tongue protraction, followed by a period of relatively stable gape angle during extraoral tongue protraction and retraction, followed by a period of rapid mouth closure), a tongue-extension cycle (protraction and retraction), and anterior head–body displacement. Among the six species, two distinct modes of prey capture are evident: (1) the Ambystoma mode (A. californiense, A. macrodactylum, A. mabeei, and A. texanum), and (2) the Linguaelapsus mode (A. annulatum and A. cingulatum). Most differences in prey-capture kinematics between the two modes are primarily differences of degree rather than the addition or loss of unique behaviors, and include a general reduction in the gape angles and a general increase in the elapsed times associated with specific events in the Linguaelapsus mode. We hypothesize that these differences are primarily the result of a prolonged period of tongue protraction in the Linguaelapsus mode during which the glandular tongue pad is fitted to the prey. In addition to differing from each other, the gape profiles of the ambystomatid subgenera differ markedly from the 4-part gape profiles of plethodontids and salamandrids.

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Prey capture in the chain pickerel, Esox niger: correlations between feeding and locomotor behavior

Canadian Journal of Zoology ◽

10.1139/z81-149 ◽

1981 ◽

Vol 59 (6) ◽

pp. 1072-1078 ◽

Cited By ~ 38

Author(s):

David M. Rand ◽

George V. Lauder

Keyword(s):

High Speed ◽

Prey Capture ◽

Mouth Opening ◽

Predatory Behavior ◽

Jaw Movements ◽

Suction Velocity ◽

Locomotor Pattern ◽

Mechanical Unit ◽

High Speed Cinematography ◽

Locomotor Patterns

The predatory behavior of the chain pickerel Esox niger was studied by high-speed cinematography to correlate patterns of jaw bone movement with locomotor patterns. Pattern B strikes were initiated at significantly shorter distances from the prey, had higher acceleration rates, and the velocity of mouth opening and suspensorial abduction was greater than for pattern A strikes. No difference was found in the excursion amplitudes of jaw movements between pattern A and pattern B strikes. Significant differences were found between midwater and corner strikes in the amplitude of mouth opening and hyoid depression: both were smaller in corner attacks and suction velocity was higher. Both velocity and amplitude of each mechanical unit in the head can be varied depending on the locomotor pattern and the position of the prey.

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Kinematics of prey capture in a flatfish, Pleuronichthys verticalis

Journal of Experimental Biology ◽

10.1242/jeb.198.5.1173 ◽

1995 ◽

Vol 198 (5) ◽

pp. 1173-1183 ◽

Cited By ~ 2

Author(s):

A Gibb

Keyword(s):

High Speed ◽

Prey Capture ◽

Mouth Opening ◽

Significant Degree ◽

The Body ◽

Bilateral Asymmetry ◽

Ocular Side ◽

Functional Features ◽

Prey Capture Behavior ◽

Pleuronichthys Verticalis

Hornyhead turbot, Pleuronichthys verticalis (Pleuronectiformes: Pleuronectidae), are morphologically asymmetrical teleosts with substantial bilateral asymmetry in the neurocranium, suspensorium and anterior jaws. In order to quantify the kinematics of prey capture and to test for functional bilateral asymmetries, four individuals of this species were video-taped feeding using a high-speed video system at 200 fields s-1. Frame-by-frame analysis revealed several features not commonly found in prey capture behavior of previously studied ray-finned fishes. These features include (1) extreme lateral compression of the suspensorium and opercular series prior to mouth opening, indicating the consistent presence of a preparatory phase during feeding, (2) apparent dissociation of hyoid retraction and lower jaw depression, (3) prolonged hyoid retraction throughout much of the feeding cycle, and (4) concomitant dorsal rotation of the neurocranium and closing of the jaws. P. verticalis also demonstrate a significant degree of functional bilateral asymmetry during prey capture. When approaching prey, fish flex their heads towards the ocular (anatomically the right) side of the body. During prey capture, their jaws bend out of the midline towards the blind (left) side. Comparisons of the displacement and timing for movements of homologous anatomical features on the ocular and blind sides of the head reveal that maximum gape is always larger on the blind side of the head than on the ocular side. In contrast, other kinematic variables measured are similar on both sides of the head. These results suggest that P. verticalis possess unique functional features of prey capture behavior and that morphological bilateral asymmetry of the head and jaws is associated with, and perhaps causally related to, the functional bilateral asymmetry present during feeding.

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The Suction Feeding Mechanism in Sunfishes (Lepomis): An Experimental Analysis

Journal of Experimental Biology ◽

10.1242/jeb.88.1.49 ◽

1980 ◽

Vol 88 (1) ◽

pp. 49-72 ◽

Cited By ~ 3

Author(s):

GEORGE V. LAUDER

Keyword(s):

Negative Pressure ◽

High Speed ◽

Prey Capture ◽

Mouth Opening ◽

Positive Phase ◽

Positive Pressure ◽

Pressure Reduction ◽

Hydrodynamic Models ◽

Suction Feeding ◽

Pressure Magnitude

The process of prey capture by inertial suction was studied in three species of sunfishes (Lepomis auritus, L. macrochirus, and L. gibbosus) by the simultaneous recording of buccal and opercular cavity pressures in order to test current hydrodynamic models of feeding in fishes. Synchronous high-speed films permitted the correlation of kinematic patterns of jaw bone movement with specific pressure waveforms. Opercular cavity pressures averaged onefifth buccal pressures and pressure magnitude was correlated with prey type. Peak buccal and opercular pressures were −650 cm H2O and −150 cm H2O respectively; peak rate of pressure change was −100 cm H2O/ms. Buccal pressure magnitude varied inversely with degree of predator satiation. Opercular pressure waveforms have an initial positive phase followed by a prolonged negative phase and then a final positive phase. The initial positive pressure may be absent during slow strikes at worms. Buccal pressure waveforms show considerable variability. The modal waveform consists of a sharp negative pressure pulse followed by a positive phase and finally by another pressure reduction. Delayed opercular abduction relative to mouth cavity compression correlates with the presence of a positive buccal phase. The second buccal negative pressure is the result of rapid mouth closing causing a pressure reduction (water hammer effect) as water flow continues posteriorly. These data indicate that (1) the buccal and opercular cavities are functionally separated by a gill curtain of high resistance, (2) that inertial effects of water are important in the description of the suction feeding process, (3) that a reverse flow of water (opercular to buccal cavity) may occur during the early phase of mouth opening prior to establishment of a buccal to opercular flow regime, and (4) current models of respiratory pressure and flow pattern cannot be applied to feeding. Current hydrodynamic models of suction feeding in fishes are re-evaluated in the light of this analysis.

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Prey Capturing Dynamics and Nanomechanically Graded Cutting Apparatus of Dragonfly Nymph

Materials ◽

10.3390/ma14030559 ◽

2021 ◽

Vol 14 (3) ◽

pp. 559

Author(s):

Lakshminath Kundanati ◽

Prashant Das ◽

Nicola M. Pugno

Keyword(s):

Electron Microscopy ◽

Mechanical Properties ◽

High Speed ◽

Prey Capture ◽

High Speed Photography ◽

Sensory Organs ◽

Dragonfly Nymph ◽

Drag Forces ◽

Predatory Insects ◽

Dragonfly Nymphs

Aquatic predatory insects, like the nymphs of a dragonfly, use rapid movements to catch their prey and it presents challenges in terms of movements due to drag forces. Dragonfly nymphs are known to be voracious predators with structures and movements that are yet to be fully understood. Thus, we examine two main mouthparts of the dragonfly nymph (Libellulidae: Insecta: Odonata) that are used in prey capturing and cutting the prey. To observe and analyze the preying mechanism under water, we used high-speed photography and, electron microscopy. The morphological details suggest that the prey-capturing labium is a complex grasping mechanism with additional sensory organs that serve some functionality. The time taken for the protraction and retraction of labium during prey capture was estimated to be 187 ± 54 ms, suggesting that these nymphs have a rapid prey mechanism. The Young’s modulus and hardness of the mandibles were estimated to be 9.1 ± 1.9 GPa and 0.85 ± 0.13 GPa, respectively. Such mechanical properties of the mandibles make them hard tools that can cut into the exoskeleton of the prey and also resistant to wear. Thus, studying such mechanisms with their sensory capabilities provides a unique opportunity to design and develop bioinspired underwater deployable mechanisms.

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The benefits of planar circular mouths on suction feeding performance

Journal of The Royal Society Interface ◽

10.1098/rsif.2011.0904 ◽

2012 ◽

Vol 9 (73) ◽

pp. 1767-1773 ◽

Cited By ~ 14

Author(s):

Tyler Skorczewski ◽

Angela Cheer ◽

Peter C. Wainwright

Keyword(s):

Prey Capture ◽

Peak Flow ◽

Mouth Opening ◽

Suction Feeding ◽

Flow Rates ◽

Computational Fluid Dynamics Simulations ◽

Enhance Efficiency ◽

And Performance ◽

Dynamics Simulations ◽

Hydrodynamic Effects

Suction feeding is the most common form of prey capture across aquatic feeding vertebrates and many adaptations that enhance efficiency and performance are expected. Many suction feeders have mechanisms that allow the mouth to form a planar and near-circular opening that is believed to have beneficial hydrodynamic effects. We explore the effects of the flattened and circular mouth opening through computational fluid dynamics simulations that allow comparisons with other mouth profiles. Compared to mouths with lateral notches, we find that the planar mouth opening results in higher flow rates into the mouth and a region of highest flow that is positioned at the centre of the mouth aperture. Planar mouths provide not only for better total fluid flow rates through the mouth but also through the centre of the mouth near where suction feeders position their prey. Circular mouths are shown to provide the quickest capture times for spherical and elliptical prey because they expose the prey item to a large region of high flow. Planar and circular mouths result in higher flow velocities with peak flow located at the centre of the mouth opening and they maximize the capacity of the suction feeders to exert hydrodynamic forces on the prey.

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Kinematics of Tongue Projection in Chamaeleo Oustaleti

Journal of Experimental Biology ◽

10.1242/jeb.159.1.109 ◽

1991 ◽

Vol 159 (1) ◽

pp. 109-133 ◽

Cited By ~ 10

Author(s):

PETER C. WAINWRIGHT ◽

DAVID M. KRAKLAU ◽

ALBERT F. BENNETT

Keyword(s):

High Speed ◽

Prey Capture ◽

Maximum Velocity ◽

Head Movements ◽

Florida State University ◽

State University ◽

Maximum Acceleration ◽

Related Family ◽

High Speed Cinematography ◽

Tongue Movements

The kinematics of prey capture by the chamaeleonid lizard Chamaeleo oustaleti were studied using high-speed cinematography. Three feeding sequences from each of two individuals were analyzed for strike distances of 20 and 35 cm, at 30°C. Ten distances and angles were measured from sequential frames beginning approximately 0.5 s prior to tongue projection and continuing for about 1.0 s. Sixteen additional variables, documenting maximum excursions and the timing of events, were calculated from the kinematic profiles. Quantified descriptions of head, hyoid and tongue movements are presented. Previously unrecognized rapid protraction of the hyobranchial skeleton simultaneously with the onset of tongue projection was documented and it is proposed that this assists the accelerator muscle in powering tongue projection. Acceleration of the tongue occurred in about 20ms, reaching a maximum acceleration of 486 m s−2 and maximum velocity of 5.8m s−1 in 35 cm strikes. Deceleration of the tongue usually began within 5 ms before prey contract and the direction of tongue movement was reversed within 10 ms of prey contact. Retraction of the tongue, caused by shortening of the retractor muscles, reached a maximum velocity of 2.99 ms−1 and was complete 330 ms after prey contact. Projection distance influences many aspects of prey capture kinematics, particularly projection time, tongue retraction time and the extent of gape and head movements during tongue retraction, all of which are smaller in shorter feedings. Though several features of the chameleon strike have apparently been retained from lizards not capable of ballistic tongue projection, key differences are documented. Unlike members of a related family, the Agamidae, C. oustaleti uses no body lunge during prey capture, exhibits gape reduction during tongue projection and strongly depresses the head and jaws during tongue retraction. Note: Present address: Department of Biological Sciences, Florida State University, Tallahassee, FL 32306, USA.

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Kinematic analysis of tongue movements during chemosensory behaviour in the European green lizard, Lacerta viridis (Reptilia: Lacertidae)

Canadian Journal of Zoology ◽

10.1139/z92-257 ◽

1992 ◽

Vol 70 (10) ◽

pp. 1886-1896 ◽

Cited By ~ 11

Author(s):

Véronique Goosse ◽

Vincent L. Bels

Keyword(s):

High Speed ◽

Prey Capture ◽

Principal Component ◽

Upward Movement ◽

High Speed Cinematography ◽

Tongue Movements ◽

Lacerta Viridis ◽

Tongue Flicking ◽

Stationary Interval ◽

Tongue Displacement

High-speed cinematography (100 frames/s) was used to allow quantitative analysis of the kinematic profiles of tongue and jaw displacements during chemosensory activities in the scleroglossan lizard Lacerta viridis. The types of tongue flicking were simple downward extensions (SDE), single oscillations (SOC), and submultiple oscillations (SMOC) of the tongue out of the mouth. The SMOC type involves a downward or upward movement of the tongue performed before a typical oscillation and it is therefore suggested that this is an intermediate category of flick between the typical SOC and MOC of lizards. Closing and opening of the mouth in SDE, SOC, and SMOC cycles may or may not be separated by a stationary stage during which the jaws are held open at a constant gape. The duration of this stationary interval increases from SDE to SMOC. Gape cycles do not show any division into slow and fast stages. The gape is produced largely by depression of the lower jaw; the upper jaw is slightly elevated by protrusion of the tongue. Patterns of correlation of kinematic variables depicting jaw and tongue movements differed between SDE, SOC, and SMOC. A principal component analysis shows that the three flick types overlap in a multivariate space constructed from the kinematic variables depicting jaw and tongue displacements. Overlap between SOC and SMOC categories is greater than that between SOC, SMOC, and SDE categories. The kinematic patterns of tongue displacement during SMOC in Lacerta viridis show similarities with those of MOC in other lizards and in snakes. Kinematically, the pattern of jaw and tongue displacements of Lacerta viridis during chemosensory activities shows similarities with those that occur during drinking and prey capture.

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The kinematics and mechanism of prey capture in the African pig-nosed frog (Hemisus marmoratum): description of a radically divergent anuran tongue.

Journal of Experimental Biology ◽

10.1242/jeb.198.9.2025 ◽

1995 ◽

Vol 198 (9) ◽

pp. 2025-2040 ◽

Cited By ~ 4

Author(s):

D Ritter ◽

K Nishikawa

Keyword(s):

Feeding Behavior ◽

Strong Evidence ◽

Muscle Function ◽

High Speed ◽

Prey Capture ◽

Three Dimensions ◽

Muscle Denervation ◽

Genioglossus Muscle ◽

Pulling Forces ◽

Hydraulic Mechanism

High-speed videography and muscle denervation experiments were used to quantify the feeding kinematics of Hemisus marmoratum and to test hypotheses of muscle function. The feeding behavior of H. marmoratum, which feeds on ants and termites, differs radically from that of other frogs that have been studied. During feeding in H. marmoratum, the tongue 'telescopes' straight out of the mouth, as opposed to the 'flipping' tongue trajectory observed in most other frogs. At the time of prey contact, two lateral lobes of tissue at the tongue tip envelop the prey. These lateral lobes are capable of applying significant pulling forces to the prey and the tongue is, therefore, described as prehensile. The trajectory of the tongue can be adjusted throughout protraction so that the frog can 'aim' its tongue in all three dimensions; distance, azimuth and elevation. Bilateral denervation of the genioglossus muscles results in a complete lack of tongue protraction, indicating that the genioglossus muscle is the main tongue protractor in H. marmoratum, as in other frogs. Thus, H. marmoratum provides strong evidence of functional conservatism of the genioglossus muscle within anurans. Bilateral denervation of the hyoglossus muscle indicates that although the hyoglossus is involved in several aspects of normal tongue retraction, including the prehensile capability of the tongue tip, it is not necessary for tongue retraction. Unilateral denervation of the genioglossus muscle causes significant deviation of the tongue towards the denervated side, providing evidence for a mechanism of lateral tongue aiming. On the basis of the kinematics of prey capture, the anatomy of the tongue and the results of the denervation experiments, we propose that H. marmoratum uses a hydraulic mechanism to protract its tongue.

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