Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes)

SummaryThe feeding mechanisms of four species of the teleostean family Labridae (Cheilinus fasciatus, C. trilobatus, Oxycheilinus bimaculatus, and O. unifasciatus) were modeled using four-bar linkage theory from mechanical engineering. The predictions of four-bar linkage models regarding the kinematics of feeding were compared to the movements observed with high speed cinematography (200 frames/s). A four-bar linkage was an accurate model of the mechanism by which upper jaw protrusion, maxillary rotation, and gape increase occur in each species. A four-bar mechanism of hyoid depression was an accurate predictor of hyoid depression when simultaneous cranial elevation and sternohyoideus contraction were simulated. Morphometrics of the linkage systems of the jaws and hyoid were collected for 12 labrid species. These data were used to calculate the transmission of force and motion through the musculoskeletal linkages. Several measures of mechanical advantage and displacement advantage were compared, including both traditional lever ratios and transmission coefficients of four-bar linkages. Alternative designs of the feeding mechanisms maximize force or velocity for the capture of different prey types. High velocity transmission of both the jaw and hyoid systems is characteristic of those species that feed on evasive prey, whereas species that feed on benthic invertebrates favor increased force transmission in both systems. Quantitative models of biomechanical systems supply criteria for functionally relevant morphometrics, and aid in calculating the capacity for transmission of force and velocity in musculoskeletal systems.

[1]  K. Liem.  Modulatory multiplicity in the functional repertoire of the feeding mechanism in cichlid fishes. I. Piscivores , 1978, Journal of morphology.

[2]  M. Muller,et al.  Optimization principles applied to the mechanism of neurocranium levation and mouth bottom depression in bony fishes (Halecostomi). , 1987 .

[3]  P. Wainwright.  Biomechanical limits to ecological performance: mollusc‐crushing by the Caribbean hogfish, Lachnolaimus maximus (Labridae) , 1987 .

[4]  Mark W. Westneat,et al.  Linkage Biomechanics and Evolution of the Unique Feeding Mechanism of Epibulus Insidiator (Labridae: Teleostei) , 1991 .

[5]  G. C. Anker.  Analyses of Respiration and Feeding Movements of the Three-Spined Stickleback, Gasterosteus Aculeatus L , 1977 .

[6]  R. M. Alexander,et al.  Elastic mechanisms in animal movement , 1988 .

[7]  K. Liem.  Adaptive Significance of Intra- and Interspecific Differences in the Feeding Repertoires of Cichlid Fishes , 1980 .

[8]  W. Kier,et al.  Tongues, tentacles and trunks: the biomechanics of movement in muscular‐hydrostats , 1985 .

[9]  M. F. Mickevich,et al.  Congruence Between Morphological and Allozyme Data in Evolutionary Inference and Character Evolution , 1976 .

[10]  C. Barel.  Towards a constructional morphology of cichlid fishes (Teleostei, Perciformes) , 1982 .

[11]  E. Otten.  The Jaw Mechanism During Growth of a Generalized Haplochromis Species: H. Elegans Trewavas 1933 (Pisces, Cichlidae) , 1982 .

[12]  Predicting patterns of prey use from morphology of fishes , 1995 .

[13]  G. Lauder.  PRESSURE AND WATER FLOW PATTERNS IN THE RESPIRATORY TRACT OF THE BASS (MICROPTERUS SALMOIDES) , 1984 .

[14]  Kirk R. Johnson,et al.  Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis. , 1987, American journal of physical anthropology.

[15]  James W. Archie,et al.  METHODS FOR CODING VARIABLE MORPHOLOGICAL FEATURES FOR NUMERICAL TAXONOMIC ANALYSIS , 1985 .

[16]  John A. Hrones,et al.  Analysis of the Four-Bar Linkage: Its Application to the Synthesis of Mechanisms , 1951 .

[17]  Q. Bone,et al.  Contractile properties and ultrastructure of three types of muscle fibre in the dogfish myotome , 1986, Journal of Muscle Research & Cell Motility.

[18]  M. Sano,et al.  Food Habits of Teleostean Reef Fishes in Okinawa Island, Southern Japan , 1985 .

[19]  J. Randall,et al.  Food habits of the giant humphead wrasse,Cheilinus undulatus (Labridae) , 1978, Environmental Biology of Fishes.

[20]  P. Wainwright,et al.  Predicting patterns of prey use from morphology of fishes , 1995, Environmental Biology of Fishes.

[21]  M. Westneat,et al.  Feeding mechanics of teleost fishes (Labridae; Perciformes): A test of four‐bar linkage models , 1990, Journal of morphology.

[22]  N. Curtin,et al.  Power Output and Force-velocity Relationship of Live Fibres from White Myotomal Muscle of the Dogfish, Scyliorhinus Canicula , 2022 .

[23]  M. Muller.  A quantitative theory of expected volume changes of the mouth during feeding in teleost fishes , 1989 .

[24]  R. German,et al.  Growth allometry of craniomandibular muscles, tendons, and bones in the laboratory rat (Rattus norvegicus): relationships to oromotor maturation and biomechanics of feeding. , 1988, The American journal of anatomy.

[25]  K. Hiiemae.  The structure and function of the jaw muscles in the rat (Rattus norvegicus L.) , 1971 .

[26]  S. Wainwright.  Axis and Circumference: The Cylindrical Shape of Plants and Animals , 1988 .

[27]  M. Westneat.  Phylogenetic relationships of the tribe cheilinini (Labridae: Perciformes) , 1993 .

[28]  Peter C Wainwright,et al.  Feeding mechanism of Epibulus insidiator (Labridae; Teleostei): Evolution of a novel functional system , 1989, Journal of morphology.

[29]  W. Weijs,et al.  Electromyography and mechanics of mastication in the albino rat , 1975, Journal of morphology.

[30]  J. Osse.  Functional Morphology of the Head of the Perch (Perca Fluviatilis L.): an Electromyographic Study , 1968 .

[31]  P. Motta.  Functional morphology of the head of the inertial suction feeding butterflyfish, Chaetodon miliaris (perciformes, chaetodontidae) , 1982, Journal of morphology.

[32]  G. Lauder.  Intraspecific Functional Repertoires in the Feeding Mechanism of the Characoid Fishes Lebiasina, Hoplias and Chalceus , 1981 .

[33]  P. Wainwright.  MORPHOLOGY AND ECOLOGY: FUNCTIONAL BASIS OF FEEDING CONSTRAINTS IN CARIBBEAN LABRID FISHES' , 1988 .

[34]  John Anthony Hrones,et al.  Analysis of the four-bar linkage , 1951 .

[35]  G. Lauder.  Evolution of the feeding mechanism in primitive actionopterygian fishes: A functional anatomical analysis of Polypterus, Lepisosteus, and Amia , 1980, Journal of morphology.