Skip to main content Accessibility help
×
Home
Hostname: page-component-55597f9d44-t4qhp Total loading time: 0.447 Render date: 2022-08-10T23:41:44.366Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "useRatesEcommerce": false, "useNewApi": true } hasContentIssue true

Article contents

A biomechanical model of feeding kinematics for Dunkleosteus terrelli (Arthrodira, Placodermi)

Published online by Cambridge University Press:  08 April 2016

Philip S. L. Anderson
Affiliation:
Department of Geophysical Sciences, University of Chicago, Chicago, Illinois 60637
Mark W. Westneat
Affiliation:
Department of Zoology, Field Museum of Natural History, Chicago, Illinois 60605

Abstract

Biomechanical models illustrate how the principles of physics and physiology determine function in organisms, allowing ecological inferences and functional predictions to be based on morphology. Dynamic lever and linkage models of the mechanisms of the jaw and skull during feeding in fishes predict function from morphology and have been used to compare the feeding biomechanics of diverse fish groups, including fossil taxa, and to test ideas in ecological morphology. Here we perform detailed computational modeling of the four-bar linkage mechanism in the skull and jaw systems of Dunkleosteus terrelli, using software that accepts landmark morphological data to simulate the movements and mechanics of the skull and jaws during prey capture. The linkage system is based on the quadrate and cranio-thoracic joints: Cranial elevation around the cranio-thoracic joint forces the quadrate joint forward, which, coupled with a jaw depressor muscle connecting the jaw to the thoracic shield, causes the jaw to rotate downward during skull expansion. Results show a high speed transmission for jaw opening, producing a rapid expansion phase similar to that in modern fishes that use suction during prey capture. During jaw closing, the model computes jaw and skull rotation and a series of mechanical metrics including effective mechanical advantage of the jaw lever and kinematic transmission of the skull linkage system. Estimates of muscle cross-sectional area based on the largest of five specimens analyzed allow the bite force and strike speed to be estimated. Jaw-closing muscles of Dunkleosteus powered an extraordinarily strong bite, with an estimated maximal bite force of over 6000 N at the jaw tip and more than 7400 N at the rear dental plates, for a large individual (10 m total length). This bite force capability is among the most powerful bites in animals. The combination of rapid gape expansion and powerful bite meant that Dunkleosteus terrelli could both catch elusive prey and penetrate protective armor, allowing this apex predator to potentially eat anything in its ecosystem, including other placoderms.

Type
Articles
Information
Paleobiology , Volume 35 , Issue 2 , Spring 2009 , pp. 251 - 269
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aerts, P., Osse, J. W. M., and Verraes, W. 1987. Model of jaw depression during feeding in Astatotilapia elegans (Teleostei: Cichlidae): Mechanisms for energy storage and triggering. Journal of Morphology 194:85109.CrossRefGoogle ScholarPubMed
Alexander, R. M. 1989. Mechanics of fossil vertebrates. Journal of the Geological Society, London 146:4152.CrossRefGoogle Scholar
Alexander, R. M. 1996. Optima for animals, 2d ed. Princeton University Press, Princeton, N.J. Google Scholar
Allis, E. P. 1923. The cranial anatomy of Chlamydoselachus anguineus . Acta Zoologica 4:123221.CrossRefGoogle Scholar
Anderson, P. S. L. 2008. Cranial muscle homology across modern gnathostomes. Biological Journal of the Linnean Society 94:195216.CrossRefGoogle Scholar
Anderson, P. S. L., and LaBarbera, M. 2008. Functional consequences of tooth design: effects of blade shape on energetics of cutting. Journal of Experimental Biology 211:36193626.CrossRefGoogle ScholarPubMed
Anderson, P. S. L., and Westneat, M. W. 2007. Feeding mechanics and bite force modelling of the skull of Dunkleosteus terrelli, an ancient apex predator. Biology Letters 3:7679.CrossRefGoogle ScholarPubMed
Anker, G. C. 1974. Morphology and kinetics of the stickleback, Gasterosteus aculeatus . Transactions of the Zoological Society, London 32:311416.CrossRefGoogle Scholar
Ashley-Ross, M. A., and Gillis, G. B. 2002. A brief history of vertebrate functional morphology. Integrative and Comparative Biology 42:183189.CrossRefGoogle ScholarPubMed
Barel, C. D. N. 1983. Toward a constructional morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology 33:357424.CrossRefGoogle Scholar
Bellwood, D. R. 2003. Origins and escalation of herbivory in fishes: A functional perspective. Paleobiology 29:7183.2.0.CO;2>CrossRefGoogle Scholar
Benton, M. J. 2005. Vertebrate Palaeontology. Blackwell, Oxford.Google Scholar
Binder, W. J., and Van Valkenburgh, B. V. 2000. Development of bite strength and feeding behavior in juvenile spotted hyenas (Crocuta crocuta). Journal of Zoology 252:273283.CrossRefGoogle Scholar
Blob, R. W. 1998. Mechanics of nonparasagittal locomotion in Alligator and Iguana: functional implications for the evolution of nonsprawling posture in the Therapsida. . University of Chicago, Chicago.Google Scholar
Blob, R. W. 2001. Evolution of hindlimb posture in nonmammalian therapsids: biomechanical tests of paleontological hypotheses. Paleobiology 27:1438.2.0.CO;2>CrossRefGoogle Scholar
Blob, R. W., and Biewener, A. A. 1999. In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and nonsprawling limb posture. Journal of Experimental Biology 202:10231046.Google ScholarPubMed
Blob, R. W., and Biewener, A. A. 2001. Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). Journal of Experimental Biology 204:10991122.Google Scholar
Bone, Q., Johnston, I. A., Pulsford, A., and Ryan, K. P. 1986. Contractile properties and ultrastructure of three types of muscle fiber in the dogfish myotome. Journal of Muscle Research and Cell Motility 7:4756.CrossRefGoogle Scholar
Brazeau, M. D. 2009. The braincase and jaws of a Devonian “acanthodian” and modern gnathostome origins. Nature (in press).Google Scholar
Carr, R. K. 1995. Placoderm diversity and evolution. In Arsenault, M., Lelievre, H., and Janvier, P., eds. Studies on early vertebrates. (VIIth International Symposium, 1991, Miguasha Parc, Quebec.) Bulletin du Museum National d'Histoire Naturelle, Paris, 4e série, C 17(1–4):85125.Google Scholar
Carroll, A. M., Wainwright, P. C., Huskey, S. H., Collar, D. C., and Turingan, R. G. 2004. Morphology predicts suction feeding performance in centrarchid fishes. Journal of Experimental Biology 207:38733881.CrossRefGoogle ScholarPubMed
Coates, M. I., and Sequeira, S. E. K. 1998. The braincase of a primitive shark. Transactions of the Royal Society of Edinburgh (Earth Sciences) 89:6385.CrossRefGoogle Scholar
Cowan, R. 1975. ‘Flapping valves’ in brachiopods. Lethaia 8:2329.CrossRefGoogle Scholar
Cowan, R. 1979. Functional Morphology. Pp. 487489 in Fairbridge, R. and Jablonski, D., eds. Encyclopedia of paleontology. Dowden, Hutchinson, and Ross, Stroudsburg, Penn. CrossRefGoogle Scholar
Curtin, N. A., and Woledge, R. C. 1988. Power output and forcevelocity relationship of live fibres from white myotomal muscle of the dogfish, Scyliorhinus canicula. Journal of Experimental. Biology 140:187197.Google Scholar
DeMar, R. E. 1976. Functional morphological models: evolutionary and non-evolutionary. Fieldiana (Geology) 33:339354.Google Scholar
Denison, R. H. 1978. Placodermi. Part. 2 of Schultze, H.-P., ed. Handbook of paleoichthyology. Gustav Fischer, Stuttgart.Google Scholar
Durie, C. J., and Turingan, R. G. 2004. The effects of opercular linkage disruption on prey capture kinematics in the teleost fish Sarotherodon melanotheron . Journal of Experimental Zoology 30:642653.CrossRefGoogle Scholar
Erickson, G. M., Van Kirk, S. D., Su, J., Levenston, M. E., Caler, W. E., and Carter, D. R. 1996. Bite-force estimation for Tyranno-saurus rex from tooth-marked bones. Nature 382:706708.CrossRefGoogle Scholar
Erickson, G. M., Lappin, A. K., and Vliet, K. A. 2003. The ontogeny of bite-force performance in American alligator (Alligator mississippiensis). Journal of Zoology 260:317327.CrossRefGoogle Scholar
Feldmann, R. M., and Hackathorn, M. 1996. Fossils of Ohio. Ohio Geological Survey Bulletin 70.Google Scholar
Ferry-Graham, L. A., and Lauder, G. V. 2001. Aquatic prey capture in ray-finned fishes: a century of progress and new directions. Journal of Morphology 248:99119.CrossRefGoogle ScholarPubMed
Gatesy, S. M., and Baier, D. B. 2005. The origin of the avian flight stroke: a kinematic and kinetic perspective. Paleobiology 31:382399.CrossRefGoogle Scholar
Gaudin, T. J., Carrano, M. T., Blob, R. W., and Wible, J. R. 2006. Introduction. Pp. 117 in Carrano, M. T., Gaudin, T. J., Blob, R. W., and Wible, J. R., eds. Amniote paleobiology. University of Chicago Press, Chicago.Google Scholar
Goujet, D. 2001. Placoderms and basal gnathostome apomorphies. In Ahlberg, P. E., ed. Major events in early vertebrate evolution: palaeontology, phylogeny, genetics and development. Systematics Association Special Volume 61:209222. Taylor and Francis, London.Google Scholar
Gould, S. J. 2002. The structure of evolutionary theory. Harvard University Press, Cambridge.Google Scholar
Gould, S. J., and Lewontin, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London B 205:581598.CrossRefGoogle Scholar
Gross, W. 1967. Uber das gebiss der Acanthodier und Placodermen. Journal of the Linnean Society (Zoology) 47:121130.Google Scholar
Huber, D. R., Eason, T. G., Hueter, R. E., and Motta, P. J. 2005. Analysis of the bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci . Journal of Experimental Biology 208:35533571.CrossRefGoogle ScholarPubMed
Janvier, P. 1996. Early vertebrates. Clarendon, Oxford.Google Scholar
Johanson, Z. 2003. Placoderm branchial and hypobranchial muscle and origins in jawed vertebrates. Journal of Vertebrate Paleontology 23:735749.CrossRefGoogle Scholar
Kammerer, C. F., Grande, L., and Westneat, M. W. 2006. Comparative and developmental functional morphology of the jaws of living and fossil gars (Actinopterygii: Lepisosteidae). Journal of Morphology 267:10171031.CrossRefGoogle Scholar
Labandeira, C. C. 1997. Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics 28:153193.CrossRefGoogle Scholar
Lauder, G. V. 1980. Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia . Journal of Morphology 163:283317.CrossRefGoogle ScholarPubMed
Lauder, G. V. 1995. On the inference of function from structure. Pp. 118 in Thomason, 1995.Google Scholar
Lauder, G. V., and Prendergast, T. 1992. Kinematics of aquatic prey capture in the snapping turtle Chelydra serpentina . Journal of Experimental Biology 164:5578.Google Scholar
Long, J. A. 1995. A new plourdosteid arthrodire from the upper Devonian Gogo formation of Western Australia. Palaeontology 38:3962.Google Scholar
Long, J. A. 1997. Ptyctodontid fishes (Vertebrata, Placodermi) from the Late Devonian Gogo Formation, Western Australia, with a revision of the European genus Ctenurella Orvig, 1960. Geodiversitas 19:515555.Google Scholar
Lucas, P. W. 2004. Dental functional morphology: how teeth work. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Medler, S. 2002. Comparative trends in shortening velocity and force production in skeletal muscles. American Journal of Physiology 283:R368R378.Google ScholarPubMed
Miles, R. S. 1969. Features of placoderm diversification and the evolution of the Arthrodire feeding mechanism. Transactions of the Royal Society of Edinburgh 68:123170.CrossRefGoogle Scholar
Miles, R. S., and Westoll, T. S. 1968. The placoderm fish Coccosteus cuspidatus Miller ex Agassiz from the Middle old red Sandstone of Scotland, Part 1. Descriptive morphology. Transactions of the Royal Society of Edinburgh 67:373476.CrossRefGoogle Scholar
Motta, P. J., Hueter, R. E., Tricas, T. C., and Summers, A. P. 2002. Kinematic analysis of suction feeding in the nurse shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae). Copeia 2002:2438.CrossRefGoogle Scholar
Muller, M. 1987. Optimization principles applied to the mechanism of neurocranium levation and mouth bottom depression in bony fishes (Halecostomi). Journal of Theoretical Biology 126:343368.CrossRefGoogle Scholar
Muller, M. 1989. A quantitative theory of expected volume changes of the mouth during feeding in teleost fishes. Journal of Zoology 217:639661.CrossRefGoogle Scholar
Myhrvold, N. P., and Currie, P. J. 1997. Supersonic sauropods? Tail dynamics in the diplodocids. Paleobiology 23:393409.CrossRefGoogle Scholar
Newberry, J. S. 1873. Description of fossil fishes. Ohio Geological Survey Report 1(2):245355.Google Scholar
Nigg, B. M. 1994. General comments about modeling. Pp. 367379 in Nigg, B. M. and Herzog, W., eds. Biomechanics of the musculo-skeletal system. Wiley, Chichester, U.K. Google Scholar
Niklas, K. J. 1994. Morphological evolution through complex domains of fitness. Proceedings of the National Academy of Sciences USA 91:67726779.CrossRefGoogle Scholar
Padian, K. 1991. Pterosaurs: were they functional birds or functional bats? Pp. 145160 in Rayner, J. M. V. and Wootton, R. J., eds. Biomechanics in evolution (Society for Experimental Biology Seminar Series 36). Cambridge University Press, Cambridge.Google Scholar
Plotnick, R. E., and Baumiller, T. K. 2000. Invention by evolution: functional analysis in paleobiology. In Erwin, D. H. and Wing, S. L., eds. Deep time: Paleobiology's perspective. Paleobiology 26(Suppl. to No. 4):305323.CrossRefGoogle Scholar
Radinsky, L. B. 1987. The evolution of vertebrate design. University of Chicago Press, Chicago.Google Scholar
Ross, C. F. 1999. How to carry out functional morphology. Evolutionary Anthropology 7:217222.3.0.CO;2-9>CrossRefGoogle Scholar
Rudwick, M. J. S. 1964. The inference of function from structure in fossils. British Journal for the Philosophy of Science 15:2740.CrossRefGoogle Scholar
Sanford, C. P. J., and Wainwright, P. C. 2002. Use of sonomicrometry demonstrates link between prey capture kinematics and suction pressure in largemouth bass. Journal of Experimental Biology 205:34453457.Google ScholarPubMed
Seilacher, A., and LaBarbera, M. 1995. Ammonites as Cartesian divers. Palaios 10:493506.CrossRefGoogle Scholar
Shockey, B. J., Croft, D. A., and Anaya, F. 2007. Analysis of function in the absence of extant functional homologues: a case study using mesotheriid notoungulates (Mammalia). Paleobiology 33:227247.CrossRefGoogle Scholar
Signor, P. W. 1982. Resolution of life habitats using multiple morphologic criteria: shell form and life habits in turritelliform gastropods. Paleobiology 8:378388.CrossRefGoogle Scholar
Stanley, S. M. 1970. Relation of shell form to life habits in the Bivalvia (Mollusca). Geological Society of America Memoir 125.Google Scholar
Thomason, J. J., ed. 1995. Functional morphology in vertebrate paleontology. Cambridge University Press, Cambridge.Google Scholar
Trinajstic, K. M., and Hazelton, M. 2007. Ontogeny, phenotypic variation and phylogenetic implications of arthrodires of the Gogo Formation, Western Australia. Journal of Vertebrate Paleontology 27:571583.CrossRefGoogle Scholar
Van Wassenbergh, S., Herrel, A., Adrians, D., and Aerts, P. 2004. Effects of jaw adductor hypertrophy on buccal expansions during feeding of air breathing catfishes (Teleostei, Clariidae). Zoomorphology 123:8193.CrossRefGoogle Scholar
Vogel, S. 1998. Cats' paws and catapults. Norton, New York.Google Scholar
Wainwright, P. C., and Richard, B. A. 1995. Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes 44:97113.CrossRefGoogle Scholar
Wainwright, P. C., Bellwood, D. R., Westneat, M. W., Grubich, J. R., and Hoey, A. S. 2004. A functional morphospace for labrid fishes: patterns of diversity in a complex biomechanical system. Biological Journal of the Linnean Society 82:125.CrossRefGoogle Scholar
Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. 1976. Mechanical design in organisms. Princeton University Press, Princeton, N.J. Google Scholar
Weggelaar, C. W., Huber, D. R., and Motta, P. J. 2004. Scaling of bite force in the blacktip shark Carcharhinus limbatus . Integrative and Comparative Biology 44:662.Google Scholar
Weishampel, D. B. 1995. Fossils, function and phylogeny. Pp. 3454 in Thomason, 1995.Google Scholar
Westneat, M. W. 1990. Feeding mechanics of teleost fishes (Labridae): a test of four-bar linkage models. Journal of Morphology 205:269295.CrossRefGoogle ScholarPubMed
Westneat, M. W. 1994. Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 114:103118.CrossRefGoogle Scholar
Westneat, M. W. 2003. A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223:269281.CrossRefGoogle ScholarPubMed
Westneat, M. W. 2004. Evolution of levers and linkages in the feeding mechanisms of fishes. Integrative and Comparative Biology 44:378389.CrossRefGoogle ScholarPubMed
Westneat, M. W. 2006. Skull biomechanics and suction feeding in fishes. Pp. 2976 in Shadwick, R. E. and Lauder, G. V., eds. Fish biomechanics. Academic Press, San Diego.Google Scholar
Wilga, C. D., Wainwright, P. C., and Motta, P. J. 2000. Evolution of jaw depression mechanics in aquatic vertebrates: insights from Chondrichthyes. Biological Journal of the Linnean Society 71:165185.CrossRefGoogle Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 1933 in Thomason, 1995.Google Scholar
Wroe, S., McHenry, C., and Thomason, J. 2005. Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society of London B 272:619625.CrossRefGoogle ScholarPubMed
Wroe, S., Huber, D. R., Lowry, M., McHenry, C., Moreno, K., Clausen, P., Ferrara, T. L., Cunningham, E., Dean, M. N., and Summers, A. P. 2008. Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? Journal of Zoology 276:336342.CrossRefGoogle Scholar
Zhu, M., and Schultze, H.-P. 2001. Interrelationships of basal osteichthyans. In Ahlberg, P. E., ed. Major events in early vertebrate evolution: palaeontology, phylogeny, genetics and development. Systematics Association Special Volume 61:289314. Taylor and Francis, London.Google Scholar
17
Cited by

Save article to Kindle

To save this article to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

A biomechanical model of feeding kinematics for Dunkleosteus terrelli (Arthrodira, Placodermi)
Available formats
×

Save article to Dropbox

To save this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about saving content to Dropbox.

A biomechanical model of feeding kinematics for Dunkleosteus terrelli (Arthrodira, Placodermi)
Available formats
×

Save article to Google Drive

To save this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you used this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about saving content to Google Drive.

A biomechanical model of feeding kinematics for Dunkleosteus terrelli (Arthrodira, Placodermi)
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *