Biomechanics of a convergently derived prey-processing mechanism in fishes: Evidence from comparative tongue bite apparatus morphology and raking kinematics

Journal of Experimental Biology

Volumn 211, Issue 21, 2008, Pages 3378-3391

  Konow, Nicolai ^a   Sanford, Christopher P J ^a  

^a HOFSTRA UNIVERSITY   (United States)

Author keywords

Aquatic; Behavior; Biomechanics; Feeding; Fish; Prey capture

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; COMPARATIVE STUDY; EVOLUTION; FEEDING BEHAVIOR; FISH; HISTOLOGY; IMAGE PROCESSING; JAW; PREDATION; RAINBOW TROUT; SPECIES DIFFERENCE; VIDEORECORDING;

ANIMALS; BIOMECHANICS; EVOLUTION; FEEDING BEHAVIOR; FISHES; IMAGE PROCESSING, COMPUTER-ASSISTED; JAW; MODELS, BIOLOGICAL; ONCORHYNCHUS MYKISS; PREDATORY BEHAVIOR; SPECIES SPECIFICITY; VIDEO RECORDING;

AMIA CALVA; AMIIDAE; ESOX AMERICANUS; ONCORHYNCHUS MYKISS; OSTEOGLOSSOMORPHA; OSTEOGLOSSUM BICIRRHOSUM; PISCES; SALMONIFORMES; SCLEROPAGES JARDINII; TELEOSTEI;

EID: 55649112086     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.023564     Document Type: Article

References (83)

1. Alfaro, M. E. and Herrel, A. (2001). Introduction: major issues of feeding motor control in vertebrates. Am. Zool. 41, 1243-1247.
2. Alfaro, M. E., Janovetz, J. and Westneat, M. W. (2001). Motor control across trophic strategies: muscle activity of biting and suction feeding fishes. Am. Zool. 41, 1266-1279.
3. Alfaro, M. E., Bolnick, D. I. and Wainwright, P. C. (2005). Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165, 140-154.
4. Anker, G. C. (1974). Morphology and kinetics of the head of the stickleback, Gasterosteus Aculeatus. Trans. Zool. Soc. Lond. 32, 311-416.
5. Brainerd, E. L., Gatesey, S. M., Baier, D. B. and Hedrick, T. L. (2007). Accurate 3D reconstruction of skeletal morphology and movement with CTX imaging. J. Morph. 268, 1053.
6. Carroll, A. M. (2004). Muscle activation and strain during suction feeding in the largemouth bass, Micropterus salmoides. J. Exp. Biol. 207, 983-991.
7. Carroll, A. M. and Wainwright, P. C. (2006). Muscle function and power output during suction feeding in largemouth bass, Micropterus salmoides. Comp. Biochem. Physiol. A. 143, 389-399.
8. De Visser, J. and Barel, C. D. N. (1996). Architectonic constraints on the hyoid's optimal starting position for suction feeding of fish. J. Morphol. 228, 1-18.
9. Dingerkus, G. and Uhler, L. D. (1977). Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol. 52, 229-232.
10. Drucker, E. G. and Jensen, J. S. (1991). Functional analysis of a specialized prey processing behavior: winnowing by surfperches (Teleostei: Embiotocidae). J. Morphol. 210, 267-287.
11. Ferry-Graham, L. A. and Lauder, G. V. (2001). Aquatic prey capture in ray-finned fishes: a century of progress and new directions. J. Morphol. 248, 99-119.
12. Frost, B. J. and Sanford, C. P. J. (1999). Kinematics of a novel feeding mechanism in the osteoglossomorph fish Chitala chitala: is there a prey-type effect? Zoology 102, 18-30.
13. Gillis, G. B. and Lauder, G. V. (1995). Kinemaitcs of feeding in bluegill sunfish: is there a general distinction between aquatic capture and transport behaviors? J. Exp. Biol. 198, 709-720.
14. Greene, C. W. and Greene, C. H. (1913). The skeletal musculature of the king salmon. Bull. U. S. Bureau Fish. 33, 21-60.
15. Greenwood, P. H. (1971). Hyoid and ventral gill arch musculature in osteoglossomorph fishes. Bull. Br. Mus. Nat. Hist. Zool. 22, 1-55.
16. Greenwood, P. H. (1973). Interrelationships of osteoglossomorphs. In Interrelationships of Fishes (ed. P. H. Greenwood, R. S. Miles and C. Patterson), pp. 307-332. London: Academic Press.
17. Greenwood, P. H. and Lauder, G. V. (1981). The protractor pectoralis muscle and the classification of teleost fishes. Bull. Br. Mus. Nat. Hist. Zool. 41, 213-234.
18. Grubich, J. R. (2003). Morphological convergence of pharyngeal jaw structure in durophagous perciform fish. Biol. J. Linn. Soc. Lond. 8, 147-165.
19. Grubich, J. R. (2005). Disparity between feeding performance and predicted muscle strength in the pharyngeal musculature of black drum, Pogonias cromis (Sciaenidae). Env. Biol. Fish. 74, 261-272.
20. Grubich, J. R. and Westneat, M. W. (2006). Four-bar linkage modelling in teleost pharyngeal jaws: computer simulations of bite kinetics. J. Anat. 209, 79-92.
21. Hernandez, L. P. and Motta, P. J. (1997). Trophic consequences of differential performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae). J. Zool. Lond. 243, 737-756.
22. Hilton, E. J. (2001). Tongue bite apparatus of osteoglossomorph fishes: variation of a character complex. Copeia 2001, 372-381.
23. Hilton, E. J. (2003). Comparative osteology and phylognetic systematics of fossil and living bony-tongue fishes (Actinopterygii, Teleostei; Osteoglossomorpha). Zool. J. Linn. Soc. 137, 1-100.
24. Ishiguro, N. B., Miya, M. and Nishida, M. (2003). Basal euteleostean relationships: a mitogenomic perspective on the phylogenetic reality of the "Protacanthopterygii". Mol. Phylogenet. Evol. 27, 476-488.
25. Kershaw, D. R. (1976). A structural and functional interpretation of cranial anatomy in relation to the feeding of osteoglossoid fishes and a consideration of their phylogeny. Trans. Zool. Soc. Lond. 33, 173-252.
26. Konow, N. and Sanford, C. P. J. (2008). Is a convergently derived muscle-activity pattern driving novel raking behaviors in teleost fishes? J. Exp. Biol. 211, 989-999.
27. Konow, N., Camp, A. L. and Sanford, C. P. J. (2008). Congruence between muscle activity and kinematics in a convergently derived prey-processing behavior. Integr. Comp. Biol. 48, 246-260.
28. Lauder, G. V. (1979). Feeding mechanisms in primitive teleosts and in the halecomorph fish Amia calva. J. Zool. Soc. Lond. 187, 543-578.
29. Lauder, G. V. (1980). Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. J. Morphol. 163, 283-317.
30. Lauder, G. V. (1981). Intraspecific functional repertoires in the feeding mechanism of the characoid fishes Lebiasina, Hoplias and Chalceus. Copeia 1981, 154-168.
31. Lauder, G. V. (1982). Patterns of evolution in the feeding mechanism of actinopterygian fishes Am. Zool. 22, 275-285.
32. Lauder, G. V. (1985). Aquatic feeding in lower vertebrates. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp. 210-229. Cambridge: Cambridge University Press.
33. Lauder, G. V. and Liem, K. F. (1980). The feeding mechanism and cephalic myology of Salvelinus fontinalis: form, function, and evolutionary significance. In Charrs: Salomnids of the Genus Salvelinus (ed. E. K. Balon), pp. 365-390. Netherlands: Junk Publishers.
34. Lauder, G. V. and Liem, K. F. (1983). The evolution and interrelationships of the Actinopterygian fishes. Bull. Mus. Comp. Zool. Harvard. 150, 95-197.
35. Lauder, G. V. and Reilly, S. M. (1994). Amphibian feeding behavior: comparative biomechanics and evolution. In Biomechanics of Feeding in Vertebrates: Advances in Comparative and Environmental Physiology (ed. V. Bels, M. Chardon and P. Vandewalle), pp. 163-195. Berlin: Springer-Verlag.
36. Lavoué, S. and Sullivan, J. P. (2004). Simultaneous analysis of five molecular markers provides a well-supported phylogenetic hypothesis for the living bony-tongue fishes (Osteoglossomorpha: Teleostei). Mol. Phylogenet. Evol. 33, 171-185.
37. Liem, K. F. (1984). The muscular basis of aquatic and aerial ventilation in the air-breathing teleost fish Channa. J. Exp. Biol. 113, 1-18.
38. Liem, K. F. (1985). Ventilation. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp. 185-209. Cambridge: Cambridge University Press.
39. Liem, K. F. (1990). Aquatic versus terrestrial feeding modes: possible impacts on the trophic ecology of vertebrates. Am. Zool. 30, 209-221.
40. Motta, P. J. (1984). The mechanics and functions of jaw protrusion in teleost fishes: a review. Copeia. 1984, 1-18.
41. Muller, M. (1987). Optimization principles applied to the mechanism of neurocranium levation and mouth bottom depression in bony fishes (Halecostomii). J. Theor. Biol. 126, 346-368.
42. Muller, M. (1989). A quantitative theory of expected volume changes of the mouth during feeding in teleost fishes. J. Zool. Lond. 217, 639-662.
43. Muller, M. (1996). A novel classification of planar four-bar linkages and its application to the mechanical analysis of animal systems. Proc. R. Soc. B. 351, 689-720.
44. Muller, M. and Osse, J. W. M. (1984). Hydrodynamics of suction feeding in fish. Trans. Zool. Soc. Lond. 37, 51-135.
45. Nelson, G. J. (1968). Gill arches of teleostean fishes of the division Osteoglossomorpha. Zool. J. Linn. Soc. 47, 261-277.
46. Norden, C. R. (1961). Comparative osteology of representative salmonid fishes with particular reference to the grayling (Thymallus arcticus) and its phylogeny. J. Fish. Res. Board Can. 18, 679-791.
47. Rand, D. M. and Lauder, G. V. (1981). Prey capture in the chain pickerel, Esox niger: Correlations between feeding and locomotor behaviour. Can. J. Zool. 59, 1072-1078.
48. Richard, B. A. and Wainwright, P. C. (1995). Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture J. Exp. Biol. 198, 419-433.
49. Ridewood, W. G. (1904). On the cranial osteology of the clupeoid fishes. Proc. Zool. Soc. Lond. 2, 448-493.
50. Ridewood, W.G. (1905). On the cranial osteology of the fishes of the families Osteoglossidoe, Pantodontidoe, and Phractoloemidoe. Zool. J. Linn. Soc. 29, 252-282.
51. Robinson, M. P. and Motta, P. J. (2002). Patterns of growth and the effects of scale on the feeding kinematics of the nurse shark (Ginglymostoma cirratum). J. Zool. Lond. 256, 449-462.
52. Roos, G., Leysen, H., Van Wassenbergh, S., Herrel, A., Jacobs, P., Dierick, M., Aerts, P. and Adriaens, D. (2008). Linking morphology and motion: a test of a fourbar mechanism in seahorses. Physiol. Biochem. Zool. (In press).
53. Rosen, D. E. (1974). Phylogeny and zoogeography of salmoniform fishes and relationships of Lepidogalaxias salamandroides. Bull. AMNH 153, 267-325.
54. Ross, C. F., Eckhardt, A., Herrel, A., Hylander, W. L., Metzger, K. A., Schaerlaeken, V., Washington, R. L. and Williams, S. H. (2007). Modulation of intra-oral processing in mammals and lepidosaurs. Integr. Comp. Biol. 47, 118-136.
55. Sanford, C. P. J. (2000). Salmonoid fish osteology and phylogeny (Teleostei: Salmonoidei). Theses Zoologicae 33. Liechtenstein, ARG Gantner Verlag KG.
56. Sanford, C. P. J. (2001a). The novel 'tongue-bite apparatus' in the knifefish family Notopteridae (Teleostei: Osteoglossomorpha): are kinematic patterns conserved within a clade? Zool. J. Linn. Soc. 132, 259-275.
57. Sanford, C. P. J. (2001b). Kinematic analysis of a novel feeding mechanism in the brook trout Salvelinus fontinalis (Teleostei: Salmonidae): behavioral modulation of a functional novelty. J. Exp. Biol. 204, 3905-3916.
58. Sanford, C. P. J. and Lauder, G. V. (1989). Functional morphology of the "Tongue-Bite" in the Osteoglossomorph fish Notopterus. J. Morphol. 202, 379-408.
59. Sanford, C. P. J. and Lauder, G. V. (1990). Kinematics of the tongue-bite apparatus in osteoglossomorph fishes J. Exp. Biol. 154, 137-162.
60. Sanford, C. P. J. and Wainwright, P. C. (2002). Use of sonomicrometry demonstrates the link between prey capture kinematics and suction pressure in largemouth bass. J. Exp. Biol. 205, 3445-3457.
61. Sass, G. G. and Motta, P. J. (2002). The effects of satiation on strike mode and prey capture kinematics in the largemouth bass, Micropterus salmoides. Environ. Biol. Fishes 65, 441-454.
62. Schwenk, K. and Wagner, G. P. (2000). Function and the evolution of phenotypic stability: connecting pattern to process. Am. Zool. 41, 552-563.
63. Sibbing, F. A. (1982). Pharyngeal mastication and food transport in the carp (Cyprinus carpio L.): a cineradiographic and electromyographic study. J. Morphol. 172, 223-258.
64. Stearley, R. F. and Smith, G. R. (1993). Phylogeny of the pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae. Trans. Am. Fish. Soc. 122, 1-33.
65. Stiassny, M. L. J., Parenti, L. and Johnson, G. D. (1996). Interrelationships of Fishes, 496 pp. New York: Academic Press.
66. Taverne, L. (1979). Ostéologie, Phylogenèse et Systématique des téléostéens fossiles et actuels du super ordre des Ostéoglossomorphes. Troisième partie: evolution des structures ostéologiques et conclusions générales relatives à la phylogenèse et à la systématique du super ordre. Bull. Acad. R. Belg. Cl. Sci. 43, 1-168.
67. Thys, T. (1997). Spatial variation in epaxial muscle activity during prey strike in largemouth bass (Micropterus salmoides). J. Exp. Biol. 200, 3021-3031.
68. Turingan, R. G. and Wainwright, P. C. (1993). Morphological and functional bases of durophagy in the queen triggerfish, Balistes vetula (Pisces, tetraodontiformes). J. Morphol. 215, 101-118.
69. Turingan, R. G., Wainwright, P. C. and Hensley, D. A. (1995). Interpopulation variation in prey use and feeding biomechanics in Caribbean triggerfish. Oecologia 102, 296-304.
70. Van Wassenbergh, S., Aerts, P. and Herrel, A. (2006). Scaling of suction feeding performance in the catfish Clarias gariepinus. Physiol. Biochem. Zool. 79, 43-56.
71. Van Wassenbergh, S., Herrel, A., Adriaens, D. and Aerts, P. (2005). A test of mouth-opening and hyoid-depression mechanisms during prey capture in a catfish. J. Exp. Biol. 208, 4627-4639.
72. Van Wassenbergh, S., Herrel, A., Adriaens, D. and Aerts, P. (2007). Interspecific variation in sternohyoideus muscle morphology in clariid catfishes: functional implications for suction feeding. J. Morphol. 268, 232-242.
73. Wagner, G. P. and Schwenk, K. (2000). Evolutionarily stable configurations: functional integration and the evolution of phenotypic stability. In Evolutionary Biology, Vol. 31 (ed. M. K. Hecht, R. J. MacIntyre and M. T. Clegg). New York: Kluwer Academic Press.
74. Wainwright, P. C. (2005). Functional morphology of the pharyngeal jaw apparatus. In Biomechanics of Fishes (ed. R. Shadwick and G. V. Lauder), pp. 77-101. Chicago: Elsevier.
75. Wainwright, P. C. and Turingan, R. G. (1993). Coupled versus uncoupled functional systems: motor plasticity in the queen triggerfish Balistes vetula. J. Exp. Biol. 180, 209-227.
76. Wainwright, P. C., Bellwood, D. R., Westneat, M. W., Grubichm, J. R. and Hoey, A. S. (2004). A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biol. J. Linn. Soc. Lond. 82, 1-25.
77. Westneat, M. W. (1991). Linkage biomechanics and evolution of the unique feeding mechanism of Epibulus Insidiator (Labridae: Teleostei) J. Exp. Biol. 159, 165-184.
78. Westneat, M. W. (1994). Transmission of force and velocity in the feeding mechanisms of labrid fishes. Zoomorphology 114, 103-118.
79. Westneat, M. W. (1995). Feeding, function, and phylogeny: analysis of historical biomechanics in labrid fishes using comparative methods. Syst. Biol. 44, 361-383.
80. Westneat, M. W. (2003). A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. J. Theor. Biol. 223, 269-281.
81. Westneat, M. W. (2004). Evolution of levers and linkages in the feeding mechanisms of fishes. Integr. Comp. Biol. 44, 378-389.
82. Wilga, C. D. and Sanford, C. P. (2008). Suction generation in white spotted bamboo sharks Chiloscyllium plagiosum. J. Exp. Biol. 211, 3128-3138.
83. Zar, J. H. (1999). Biostatistical Analysis, 4th edn, 663 pp. New Jersey: Prentice Hall.