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Cranial biomechanics and feeding performance of sharks

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Cranial biomechanics and feeding performance of sharks
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English
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Huber, Daniel Robert
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University of South Florida
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Elasmobranch
Functional morphology
Aquatic prey capture
Bite force
Jaw suspension
Dissertations, Academic -- Biology -- Doctoral -- USF
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non-fiction   ( marcgt )

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Abstract:
ABSTRACT: The elasmobranch fishes possess a remarkable diversity of feeding mechanisms for a group containing relatively few species (~1200). The three most prevalent of these mechanisms involve prey capture during which the predator overtakes its prey (ram), prey is drawn into the mouth of the predator (suction), and relatively stationary consumption of sessile or substrate affixed prey (biting). Biomechanical modeling of cranial force distributions, in situ bite performance trials, and kinematic analysis of prey capture behaviors were employed to identify morphological and behavioral specializations and constraints associated with these feeding mechanisms in lemon Negaprion brevirostris (ram), whitespotted bamboo Chiloscyllium plagiosum (suction), and horn Heterodontus francisci (biting) sharks. Biomechanical modeling of the forces generated by the cranial musculature was used to theoretically estimate the maximum bite force and mechanical loadings occurring throughout the hyostyl ic jaw suspension mechanisms of each species, characterized by suspensory hyomandibular cartilages between the back of the jaws and cranium and anterior ligamentous attachments. To assess the mechanical factors involved in the evolution of elasmobranch jaw suspension mechanisms, the feeding mechanism of the sharpnose sevengill shark Heptranchias perlo was modeled as well. Heptranchias perlo possesses an ancestral amphistylic jaw suspension mechanism including non-suspensory hyomandibular cartilages, a large post-orbital articulation between the jaws and cranium, and anterior ligamentous attachments. Theoretical estimates of maximum bite force were compared to voluntary bite forces measured during in situ bite performance trials. Voluntary bite force measurements allowed the quantification of discrete behavioral attributes of bite force application in each species. To further assess the behavioral specializations associated with these feeding mechanisms, high-speed digital videography w as used to analyze the prey capture cranial kinematics of species. Collectively, these analyses have developed a morphological and behavioral basis from which to understand the functional diversity of the ram, suction, and biting feeding mechanisms in elasmobranchs.
Thesis:
Dissertation (Ph.D.)--University of South Florida, 2006.
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Includes bibliographical references.
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by Daniel Robert Huber.
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Includes vita.

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ABSTRACT: The elasmobranch fishes possess a remarkable diversity of feeding mechanisms for a group containing relatively few species (~1200). The three most prevalent of these mechanisms involve prey capture during which the predator overtakes its prey (ram), prey is drawn into the mouth of the predator (suction), and relatively stationary consumption of sessile or substrate affixed prey (biting). Biomechanical modeling of cranial force distributions, in situ bite performance trials, and kinematic analysis of prey capture behaviors were employed to identify morphological and behavioral specializations and constraints associated with these feeding mechanisms in lemon Negaprion brevirostris (ram), whitespotted bamboo Chiloscyllium plagiosum (suction), and horn Heterodontus francisci (biting) sharks. Biomechanical modeling of the forces generated by the cranial musculature was used to theoretically estimate the maximum bite force and mechanical loadings occurring throughout the hyostyl ic jaw suspension mechanisms of each species, characterized by suspensory hyomandibular cartilages between the back of the jaws and cranium and anterior ligamentous attachments. To assess the mechanical factors involved in the evolution of elasmobranch jaw suspension mechanisms, the feeding mechanism of the sharpnose sevengill shark Heptranchias perlo was modeled as well. Heptranchias perlo possesses an ancestral amphistylic jaw suspension mechanism including non-suspensory hyomandibular cartilages, a large post-orbital articulation between the jaws and cranium, and anterior ligamentous attachments. Theoretical estimates of maximum bite force were compared to voluntary bite forces measured during in situ bite performance trials. Voluntary bite force measurements allowed the quantification of discrete behavioral attributes of bite force application in each species. To further assess the behavioral specializations associated with these feeding mechanisms, high-speed digital videography w as used to analyze the prey capture cranial kinematics of species. Collectively, these analyses have developed a morphological and behavioral basis from which to understand the functional diversity of the ram, suction, and biting feeding mechanisms in elasmobranchs.
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Cranial Biomechanics and Feeding Performance of Sharks by Daniel Robert Huber A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Biology College of Arts and Sciences University of South Florida Major Professor: Phi lip J. Motta, Ph.D. Robert E. Hueter, Ph.D. Thomas J. Koob, Ph.D. Florence I. Thomas, Ph.D. James R. Garey, Ph.D. Date of Approval: June 2, 2006 Keywords: elasmobranch, functiona l morphology, aquatic prey capture, bite force, jaw suspension Copyright 2006 Daniel Robert Huber

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Dedication I dedicate this work to my parents, Ma rk, Geri, Joann, and Steve, for fostering a kids bizarre fascination with dangerous animals. Their foresight and unwavering support over the past twenty-seven years has been the foundation of the perseverance and integrity that has led to the completion of my doctorate. I am fore ver indebted to them, and hope that I have made them proud.

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Acknowledgements I would first like to acknowledge the cont ributions of my mentor and friend Dr. Philip J. Motta. His wisdom in all things shar k and otherwise has been a guiding force in my life over the past six years and I cannot imagine having found a more insightful and cheerful person to call boss. Secondly, I would like to ack nowledge Christina Weggelaar, whose confidence in and patience with me have been crucial to my sanity and success. Many others have contributed to the work herein, including Drs. Thomas Eason, James Garey, Robert Hueter, Thomas K oob, Adam Summers, and Florence Thomas. Years full of thought provoking conversation and brainstorming on this and other projects were provided by Angela Collins, Eric Cross, Mason Dean, Mark Driscoll, Dayv Lowry, Kyle Mara, Mike Matott, Samantha Mulvany, Justin Schaefer, Lisa Whitenack, and Alpa Wintzer. Experimental assistance was provi ded by Dan Conklin, Coral Gehrke, Wayne Giordano, Terry Hall, Eric Hovland, Kristen Mathews, Sean Moore, Jack Morris, Wes Pratt, Chris Schreiber, and John Tyminski The use of facilities and specimens was provided by California State University at Long Beach, Florida Museum of Natural History, Florida Aquarium, Hokkaido University, Mote Marine Laboratory Center for Shark Research, Occidental College, SeaWorld Entertainment Parks, Texas A&M University, University of Miami, Univers ity of South Florida, and University of Washington Friday Harbor Laboratories. Fundi ng for this project was provided by the American Elasmobranch Society, American So ciety of Ichthyologist s and Herpetologists, Mote Marine Laboratory, PADI Project A.W.A.R.E. Foundation, Porter Family Foundation, Society for Integrative and Comp arative Biology, University of South Florida Department of Biology, and University of South Florida Foundation.

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i Table of Contents List of Tables................................................................................................................. .....iv List of Figures...................................................................................................................vii Abstract....................................................................................................................... .......xi Chapter One. Prey Capture Biomechanics and Feeding Performance of the Horn Shark Heterodontus francisci .........................................................................................1 Introduction....................................................................................................... .......3 Materials and Methods.............................................................................................6 Experimental Animals.................................................................................6 Morphological Analysis...............................................................................6 Theoretical Force Generation....................................................................10 In Situ Bite Performance Measurements....................................................12 Restrained and Stimulated Bite Force Measurements...............................14 Statistical Analysis.....................................................................................15 Results............................................................................................................ ........17 Biomechanical Modeling...........................................................................17 Performance Measurements.......................................................................22 Methodological Comparison......................................................................27 Bite Forces Among Vertebrates.................................................................28 Discussion..............................................................................................................30 Functional Morphology.............................................................................30 Methodological Comparison......................................................................37 Feeding Performance.................................................................................39 Feeding Ecology........................................................................................42 Conclusions............................................................................................................44 Chapter Two. Prey Capture Biomechanics and Feeding Performance of Juvenile Lemon Sharks Negaprion brevisostris ..........................................................................46 Introduction....................................................................................................... .....48 Materials and Methods...........................................................................................52 Experimental Animals...............................................................................52 Cranial Morphology...................................................................................52 Theoretical Biomechanical Analysis.........................................................55 Bite Performance Measurements...............................................................58 Statistical Analysis.....................................................................................60

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ii Results............................................................................................................ ........62 Cranial Biomechanics................................................................................62 Mechanics of Jaw Protrusion.....................................................................67 Prey Capture Performance.........................................................................68 Methodological Comparison......................................................................73 Bite Forces Among Cartilaginous Fishes..................................................73 Discussion..............................................................................................................71 Cranial Biomechanics................................................................................74 Mechanics and Evolution of Jaw Suspension............................................77 Prey Capture Performance.........................................................................82 Methodological Comparison......................................................................85 Conclusions............................................................................................................86 Chapter Three. Mechanical Consequences of Functional Constrai nt in the Feeding Mechanism of the Whitespotted Bamboo Shark Chiloscyllium plagiosum.................. 88 Introduction............................................................................................................90 Materials and Methods...........................................................................................95 Experimental Animals...............................................................................95 Morphological Analysis.............................................................................95 Theoretical Force Generation....................................................................98 Bite Force Measurement..........................................................................101 Statistical Analysis...................................................................................103 Results............................................................................................................ ......104 Biomechanical Modeling.........................................................................104 Methodological Comparison....................................................................110 Discussion............................................................................................................111 Functional Constraint...............................................................................111 Prey Capture.............................................................................................117 Methodological Comparison....................................................................121 Conclusions..........................................................................................................121 Chapter Four. Prey Capture Behavior and Performance of Shar ks Utilizing Ram, Suction, and Suction-Biting Feeding Methodologies.................................................123 Introduction....................................................................................................... ...125 Materials and Methods.........................................................................................129 Experimental Animals.............................................................................129 Kinematic Analysis..................................................................................130 In Situ Bite Performance Measurements..................................................131 Statistical Analysis...................................................................................132 Results............................................................................................................ ......133 Kinematic Analysis..................................................................................133 Effects of Prey Size on Capture Kinematics............................................145 Kinetic Analysis.......................................................................................146 Behavioral Canalization...........................................................................149

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iii Discussion............................................................................................................150 Ram Feeding............................................................................................151 Suction Feeding.......................................................................................157 Suction-Biting..........................................................................................160 Variability in Prey Capture Behavior......................................................163 Conclusions..........................................................................................................165 Chapter Five. Comparative Prey Capture Biomechanics of Sharks: Implications for the Evolution of Jaw Suspension Mechanisms.....................................................167 Introduction....................................................................................................... ...169 Materials and Methods.........................................................................................176 Species Descriptions................................................................................176 Morphological Analysis...........................................................................177 Theoretical Force Generation..................................................................179 Statistical Analysis...................................................................................182 Results............................................................................................................ ......183 Discussion............................................................................................................192 Prey Capture Biomechanics.....................................................................192 Jaw Suspension Mechanics......................................................................199 Evolution of Jaw Suspension...................................................................206 Jaw Suspension Mechanics in Non-Elasmobranch Fishes......................209 Conclusions..........................................................................................................212 Literature Cited............................................................................................................... .213 Appendices.......................................................................................................................231 Appendix I: Mass-Specific B ite Forces of Vertebrates.......................................232 About the Author...................................................................................................End Page

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iv List of Tables Table 1 Theoretical maximum forces generated by the cranial musculature active during the gape cycle in H. francisci ........................................18 Table 2 Resultant bilateral muscle a nd jaw forces occurring during prey capture in H. francisci broken into their principal components..........19 Table 3 Unilateral mechanical loadings at articulation points in H. franciscis feeding mechanism broken into their principal components..........................................................................................20 Table 4 In situ bite performance data for H. francisci biting at the tips of its jaws......................................................................................................23 Table 5 Principal component loadi ngs of performance and kinematic variables from bite performance trials of H. francisci ........................25 Table 6 Results of one-way ANOVA on different methods of determining bite force at the tips of the jaws in H. francisci ...................................28 Table 7 Resultant forces occurring dur ing prey capture broken into their principal components in N. brevirostris ..............................................63 Table 8 Mechanical loadings at ar ticulation points in the feeding mechanism of N. brevirostris broken into their principal force components.........................................................................................66 Table 9 In situ bite performance data for N. brevirostris ........................................69 Table 10 Principal component loadi ngs of performance and kinematic variables from bite performance trials of N. brevirostris ....................71 Table 11 Theoretical maximum forces generated by the cranial musculature during the gape cycle in C. plagiosum ..............................................106 Table 12 Resultant forces occu rring during prey capture in C. plagiosum broken into their principal components.............................................106

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v Table 13 Mechanical loadings at articulation points in the feeding mechanism of C. plagiosum broken into their principal force components.......................................................................................107 Table 14 Results of one-way ANOVA on different methods of determining bite force at the tips of the jaws in C. plagiosum ..............................110 Table 15 Principal component loadings of kinematic variables from 0.5W feeding trials of H. francisci N. brevirostris and C. plagiosum ......136 Table 16 Kinematics data from 0.5W feeding trials of H. francisci N. brevirostris and C. plagiosum ..........................................................137 Table 17 Principal component loadings of kinematic variables from 1W feeding trials of H. francisci N. brevirostris and C. plagiosum ......141 Table 18 Kinetic data from bite performance trials of H. francisci N. brevirostris and C. plagiosum ..........................................................142 Table 19 Mass-specific kinetic data from bite performance trials of H. francisci, N. brevirostris and C. plagiosum ......................................146 Table 20 Principal component loadings of bite performance variables of H. francisci, N. brevirostris and C. plagiosum ......................................147 Table 21 Mean coefficients of variation for kinematic and kinetic variable groups in H. francisci, N. brevirostris and C. plagiosum .................148 Table 22 Kinetic data from bite performance trials of H. francisci N. brevirostris and C. plagiosum ..........................................................150 Table 23 Bilateral forces produced by the cranial muscles during the expansion and compression of the feeding mechanisms of H. francisci N. brevirostris C. plagiosum and H. perlo ......................184 Table 24 Mechanical advantages and force distributions (N) during feeding in H. francisci N. brevirostris C. plagiosum and H. perlo .............185 Table 25 Resultant jaw adducting forces (N) of H. francisci N. brevirostris C. plagiosum and H. perlo broken into their principal components ......................................................................................186 Table 26 Results of principal com ponents analysis of jaw adducting and mechanical loading variables in H. francisci N. brevirostris C. plagiosum and H. perlo ....................................................................190

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vi Table 27 Hypothesized suspensorial loading regime occurring in the feeding mechanisms of the chondrichthyan fishes based upon mechanical modelin g of the feeding mechanisms of H. francisci N. brevirostris C. plagiosum and H. perlo ......................202

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vii List of Figures Figure 1. Lateral views of representa tive elasmobranch jaw suspensions..................5 Figure 2. Right lateral (A) and ventral (B) views of the cranial and branchial musculature of a 63 cm male H. francisci ..............................................7 Figure 3. Coordinate system for thre e-dimensional vector analysis and schematic diagram of the jaws of H. francisci indicating variables for mechanical lever-ratio analysis.........................................9 Figure 4. Forces involved in the static equilibrium calcula tions of the lower and upper jaws of H. francisci ..............................................................11 Figure 5. Theoretical maximum bi te force (N) of five male H. francisci .................19 Figure 6. Bite force waveforms from b ite performance trials of three male H. francisci ................................................................................................23 Figure 7. Maximum in situ bite force (N) from five male H. francisci plotted against (A) impulse (kg m s -1 ) and (B) force duration (ms) on logarithmic axes...............................................................................26 Figure 8. Bite forces (N) of various vertebrates plotted against mass (g).................29 Figure 9. Left lateral view of th e cranium, jaws, and hyoid arch of N. brevirostris with the skin and muscles removed.................................49 Figure 10. (A) Left lateral and (B) ventra l views of the cran ial musculature of N. brevirostris .......................................................................................53 Figure 11. Forces involved in the static equilibrium calcula tions of the lower and upper jaws of N. brevirostris .........................................................56 Figure 12. Theoretical forces produced by the muscles involved in (A) abduction and (B) adduction of the feeding mechanism of N. brevirostris .......................................................................................63

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viii Figure 13. Diagrammatic explanation of local versus global forces acting at articulations within the feeding mechanism of N. brevirostris ...........................................................................................65 Figure 14. Linear regressions of log 10 -transformed bite performance variables of N. brevirostris ..................................................................................70 Figure 15. Lateral Left lateral views of the feeding mechanisms of (A) the sharpnose sevengill shark Heptranchias perlo (amphistyly); (B) whitespotted bamboo shark Chiloscyllium plagiosum (hyostyly); (C) lesser electric ray Narcine brasiliensis (euhyostyly)..........................................................................................92 Figure 16. Right lateral vi ew of the cranium of C. plagiosum illustrating the constrained linkage between the orbital groove of the cranium and the orbital process of the upper jaw.................................94 Figure 17. Left lateral (A) and ventral (B) views of the cranial and branchial musculature of C. plagiosum ................................................................97 Figure 18. Schematic diagram of the jaws of C. plagiosum indicating (A) variables for lever ratio an alysis and (B) the forces involved in static equilibr ium calculations of the upper and lower jaws..........................................................................................100 Figure 19. Diagrammatic explanation of lo cal versus global forces acting at articulations within the feeding mechanism of C. plagiosum using the jaw joint as a model............................................................108 Figure 20. Right lateral view of the feeding mechanism of C. plagiosum indicating the balanc e of forces acting on the jaws (A) while the ethmoidal articulation remains intact due to the functional constraint impos ed by the association of the orbital process and orbi tal groove on the upper jaw and cranium respectively (see Materials and methods for description), and (B) wh ile the functional constraint imposed by the orbital process and orbital groove is theoretically released, allowing the upper jaw to dissociate from the cranium during protrusion of the upper jaw.....................................................113 Figure 21. Principal components analysis of expansive and compressive phase kinematic variables from capture of 0.5W sized food by H. francisci C. plagiosum and N. brevirostris .......................................135

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ix Figure 22. Principal components anal ysis of palatoquadrate protrusion kinematic variables from capture of 0.5W sized food by H. francisci C. plagiosum and N. brevirostris .......................................138 Figure 23. Principal components analysis of head depression kinematic variables from capture of 0.5W sized food by H. francisci C. plagiosum and N. brevirostris .......................................................140 Figure 24. Principal components analysis of expansive and compressive phase kinematic variables from capture of 1.0W sized food by H. francisci C. plagiosum and N. brevirostris .......................................143 Figure 25. Principal components analys is of palatoquadrate protrusion kinematic variables from capture of 1.0W sized food by H. francisci C. plagiosum and N. brevirostris .......................................145 Figure 26. Principal components analysis of kinetic variables from bite performance trials of H. francisci C. plagiosum and N. brevirostris .........................................................................................147 Figure 27. Representation of kinematic and kinetic behavioral transitions associated with capturing prey via ram, suction, and suction-biting feeding methodologies................................................152 Figure 28. Right lateral views of the feeding mechanisms of elasmobranchs with different jaw suspensions...........................................................170 Figure 29. Dorsal views of the neurocrania of the A) cladodont shark Cladodus B) sharpnose sevengill shark Heptranchias perlo, and C) shortfin mako shark Isurus oxyrinchus, illustrating the reduction of the postorbital processes during the evolutionary transition from amphistyly to hyostyly..............................................171 Figure 30. Coordinate system for threedimensional vector analysis of the forces generated by the cranial musculature represented by H. francisci ..............................................................................................178 Figure 31. Schematic diagram of the jaws of N. brevirostris indicating (A) variables for mechanical lever-ratio analysis, (B) forces involved in the static e quilibrium calculations of the lower and upper jaws, and (C) the disarticulation of the upper jaw from the cranium at maximum upper jaw protrusion.................................181

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x Figure 32. Diagrammatic explanation of local versus global forces acting at articulations within the feeding mechanism, using the jaw joint of N. brevirostris as a model..............................................................187 Figure 33. Principal components analys is of jaw adducting muscle forces, mechanical advantages, and the resulting fo rce distributions throughout the jaws and th eir articulations wi th the cranium in Heterodontus francisci Chiloscyllium plagiosum Negaprion brevirostris and Heptranchias perlo .................................................190 Figure 34. Regression analyses of react ion forces (N) occurring within the feeding mechanisms of H. francisci C. plagiosum N. brevirostris and H. perlo during prey capture...................................191 Figure 35. Right lateral views of the feeding mechanisms of (A) C. plagiosum and (B) N. brevirostris indicating the net fo rces acting on the jaws and their articulations with the cranium during biting...............201

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xi Cranial Biomechanics and Feeding Performance of Sharks Daniel Robert Huber ABSTRACT The elasmobranch fishes possess a remarkable diversity of feeding mechanisms for a group containing relatively few species (~1200). The three most prevalent of these mechanisms involve prey capture during whic h the predator overtak es its prey (ram), prey is drawn into the mouth of the pred ator (suction), and relatively stationary consumption of sessile or s ubstrate affixed prey (biting) Biomechanical modeling of cranial force distributions, in situ bite performance trials, and kinematic analysis of prey capture behaviors were employed to identify morphological and behavioral specializations and constraints associated with these feeding mechanisms in lemon Negaprion brevirostris (ram), whitespotted bamboo Chiloscyllium plagiosum (suction), and horn Heterodontus francisci (biting) sharks. Biomechani cal modeling of the forces generated by the cranial musculature was used to theoretically estimate the maximum bite force and mechanical loadings occurri ng throughout the hyostylic jaw suspension mechanisms of each species, characterize d by suspensory hyomandibular cartilages between the back of the jaws and cranium and anterior ligament ous attachments. To assess the mechanical factors involved in the evolution of elasmobranch jaw suspension mechanisms, the feeding mechanism of the sharpnose sevengill shark Heptranchias perlo was modeled as well. Heptranchias perlo possesses an ancestral amphistylic jaw

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xii suspension mechanism including non-suspenso ry hyomandibular cartilages, a large postorbital articulation between the jaws and cran ium, and anterior ligamentous attachments. Theoretical estimates of maximum bite force were compared to voluntary bite forces measured during in situ bite performance trials. Volunt ary bite force measurements allowed the quantification of discrete behavioral attributes of bite force application in each species. To further assess the behavior al specializations associated with these feeding mechanisms, high-speed digital vi deography was used to analyze the prey capture cranial kinematics of species. Coll ectively, these analyses have developed a morphological and behavioral basis from whic h to understand the functional diversity of the ram, suction, and biting feeding mechanisms in elasmobranchs.

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1 Chapter 1: Prey Capture Biomechanics and Feeding Performance of the Horn Shark Heterodontus francisci Abstract Three-dimensional static e quilibrium analysis of the fo rces generated by the jaw musculature of the horn shark Heterodontus francisci was used to theoretically estimate the maximum force distributions and loadi ngs on its jaws and suspensorium during biting. Theoretical maximum bite force was then compared to bite forces measured: (1) voluntarily in situ ; (2) in restrained animals; and (3 ) during electrical st imulation of the jaw adductor musculature of anesthetized shar ks. Maximum theoretical bite force ranged from 128 N at the anterior-most cuspidat e teeth, to 338 N at the posterior-most molariform teeth. The hyomandibula, which conn ects the posterior margin of the jaws to the base of the chondrocranium, is loaded in tension during biting. Conversely, the ethmoidal articulation between the pa latal region of the upper jaw and the chondrocranium is loaded in compression, even during upper jaw protrusion because H. franciscis upper jaw does not disarticulate from the chondrocranium during prey capture. Maximum in situ bite force averaged 95 N for free-swimming H. francisci, with a maximum of 133 N. Time to maximum force averaged 322 ms and was significantly longer than time away from maximum force (212 ms). Bite force measurements from restrained individuals (187 N) were significantly greater than those from free-swimming individuals (95 N), but equivale nt to those from both theore tical (128 N) and electrically

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2 stimulated measurements (132 N). The mean mass specific bite of H. francisci was greater than that of many ot her vertebrates and highest of the cartilaginous fishes that have been studied. Measuring bite force on re strained sharks appears to be the best indicator of maximum bite force. The large b ite forces and robust molariform dentition of H. francisci correspond to its consumption of hard prey.

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3 Introduction The elasmobranch fishes (sharks, skates, and rays) possess highly diverse feeding mechanisms composed of few kinetic elements making them an ideal group in which to investigate feeding biomechanic s and patterns of diversity in cranial morphology, feeding behavior, and ecology. Elasmobranchs inhabit ne arly all marine environments and have evolved ram, suction, biting, and filter feedi ng mechanisms to exploit prey ranging from plankton to marine mammals (Motta, 2004). Among the diverse feeding mechanisms found in extant elasmobranch taxa are t hose adapted for durophagy, the consumption of hard prey. While hard prey of some sort is found in the diets of elasmobranchs from approximately thirteen families, it does not comprise a substantial portion of the diet in many of these groups. Genuine durophagy ha s convergently evolved in the bullhead (Heterodontidae), hammerhead (Sphyrnidae), zebra (Stegostomatid ae), and hound sharks (Triakidae), as well as eagle rays (Myliobatid ae) (Compagno, 1984a, 1984b, 2001; Summers et al., 2004). The heterodontid sharks are the only fa mily of elasmobranchs in which every species is ecologically and functionally specialized for durophagy (Taylor, 1972; Compagno, 1984a, 1999). The suite of morphol ogical characters associated with durophagy in the heterodontid sharks includ es robust jaws capable of resisting dorsoventral flexion under high loading, molariform teeth, and hypertrophied jaw adductor muscles (Reif, 1976; Nobiling, 1977; Summers et al., 2004). To date, the concept of durophagy in the heterodontid shar ks has mostly been examined qualitatively (but see Summers et al. (2004)). Neither the bite forces they are cap able of producing, nor the subsequent loadings on the various arti culations within their feeding mechanisms,

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4 have been quantified in any manner. Bite force is particularly informative in regard to linking morphological, ecological, and behavioral variables associated with prey capture because biting capacity is dictated by cranial morphology and is known to affect resource partitioning (Wiersma, 2001; Verwaijen et al ., 2002), dietary diversity (Wainwright, 1988; Clifton and Motta, 1998), and ontogenetic changes in f eeding ecology (Hernandez and Motta, 1997). Like most modern elasmobr anchs, the heterodontid sh arks possess a hyostylic jaw suspension in which the mandibular arch indi rectly articulates w ith the chondrocranium via the hyomandibular cartilages, and the pa latal region of the upper jaw is suspended from the ethmoid region of the chondrocranium via ligamentous connections (Fig. 1A). However, a number of variants on this arra ngement exist, primarily in the superorder Squalea (Gregory, 1904; Shirai, 1996; Wilga, 2002). The hexanchiform sharks possess an orbitostylic jaw suspension in which the upper ja w articulates with the ethmoidal, orbital, and postorbital regions of the chondrocrani um and the hyomandibula contributes little support to the jaws (Fig. 1B). Conversely, the only suspensorial element in the batoids is the hyomandibula (euhyostyly, Fig. 1C) (G regory, 1904; Maisey, 1980; Wilga, 2002). These highly divergent morphologies consti tute independent mechanical systems, perhaps with comparably divergent cranial loading regimes occurr ing during feeding. Determining these loading regimes will help to establish the link, if any, between elasmobranch jaw suspension and the functiona l diversity of their feeding mechanisms. The purpose of this study was therefore to determine the biomechanical basis of durophagy in the heterodontid sharks, as represented by the horn shark Heterodontus

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Figure 1. Left lateral views of representative elasmobranch jaw suspensions. (A), Heterodontus, Heterodontiformes (hyostyly); (B), Heptranchias, Hexanchiformes (amphistyly); (C), Rhinobatos, Batoidea (euhyostyly). Articulation points are marked with arrows. C, ceratohyal; E, ethmoidal; H, hyomandibula; L, lower jaw; O, orbital; P, postorbital; U, upper jaw. Reproduced from Wilga (2002) with permission from Blackwell Publishing. francisci, a primarily shallow water, nocturnal forager of molluscs, echinoderms, and benthic crustaceans (Strong Jr., 1989; Segura-Zarzosa et al., 1997). Heterodontus francisci uses suction to capture prey, which is grasped by the anterior, cuspidate teeth and then crushed by the posterior molariform teeth, effectively combining both suction and biting feeding mechanisms (Edmonds et al., 2001; Summers et al., 2004). Through in situ bite performance measurements and theoretical modeling of the forces generated by 5

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6 the cranial musculature of H. francisci the specific goals of this study were to: 1) theoretically determine the forces generated by each of the crania l muscles active during the gape cycle; 2) determine the distri bution of forces throughout the jaws and suspensorium, and discuss the implications of these loadings for jaw suspension; 3) compare theoretical bite force from anat omical measures to those obtained during voluntary unrestrained feeding, restrained bi ting, and electrical stimulation of the jaw adductors; 4) relate its bite performance to feeding ecology; and 5) compare the bite force of H. francisci to those of other vertebrates. Materials and Methods Experimental Animals Five horn sharks Heterodontus francisci Girard (63 cm – 74 cm TL) were housed at the University of South Florida in Tampa, FL in accordance with the guidelines of the Institutional Animal Care and Use Co mmittee (IACUC #1882). Individuals were maintained at 20 C in a 1,500 l semicircular tank on a diet of thread herring Opisthonema oglinum and squid ( Loligo spp.). The planar face of the tank held a window for viewing. Five additional H. francisci (55 cm – 68 cm TL) obtained as fisheries bycatch off the coast of Los Angeles, CA were frozen until used for mo rphological analyses. Morphological Analysis A theoretical model of th e feeding mechanism of H. francisci was designed by investigating the forces produ ced by the nine cranial musc les involved in the abduction (coracomandibularis, coracohyoi deus, coracoarcualis, and co racobranchiales), adduction (adductor mandibulae complex consisting of the quadratomandibular is-preorbitalis

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7 Figure 2. Right lateral (A) and ventral (B) view s of the cranial and branchial musculature of a 63 cm male H. francisci CC, coracoarcualis; CH, coracohyoideus; CHD, dorsal hyoid constrictor; CHV, ventral hyoid c onstrictor; CM, coracomandibularis; CO, coracoid bar; HM, hyomandibulo-mandibularis ; IMD, intermandibularis; LH, levator hyomandibularis; LJ, lower jaw; LP, le vator palatoquadrati; QM-PO complex, quadratomandibularis-preor bitalis complex; QM, quadratomandibularis; PO, preorbitalisUJ, upper jaw; VSBC, ventral superf icial branchial constrictor. The intermandibularis (IMD) has b een partially removed to reve al the ventral musculature. The coracobranchiales (not shown) are lo cated deep to the coracoarcualis (CC).

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8 complex, quadratomandibularis, and preorbitalis) and retraction (levator palatoquadrati and levator hyomandibularis) of the jaws and hyobranchial region (Fig. 2). The quadratomandibularis-preorbitalis complex consists of six individual heads of the adductor mandibulae complex (Nobiling, 1977). Di fficulty in mechanically separating these heads led to their analysis as a group. Us ing the tip of the snout as the center of a three-dimensional coordinate system, the th ree-dimensional position of the origin and insertion of each muscle were determined by measuring the distance of these points from the respective X, Y, and Z planes intersecting the tip of the snout (Fig. 3A). Each muscle was then excised (unilaterally where applic able), bisected thr ough its center of mass perpendicular to the principal fiber direction, and digital im ages of the cross-sections were taken (JVC DVL9800 camera). Cross-se ctional areas were measured from these images using Sigma Scan Pro 4.01 (SPSS, Inc.). Center of mass was estimated by suspending the muscle from a pin and traci ng a vertical line down the muscle. After repeating this from another point, the inters ection of the two line-t racings indicated the center of mass of the muscle. The three-dimensional coordinates of the cen ter of rotation of the dual (lateral and medial (Nobiling, 1977)) quadratomandibular ja w articulation (hereafter referred to as “jaw joint”), ethmoidal arti culation, and the lateral and me dial articulations of the hyomandibula with the jaws a nd chondrocranium respectively were determined with respect to the right side of the head of each individual. Points corresponding to 0, 25, 50, 75, and 100% of the distance along the functi onal tooth row on the lower jaw from the posterior-most molariform tooth were also determined; 100% is the anterior-most cuspidate tooth. The in-lever for jaw abduction from the center of rotati on of the jaw joint

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9 Figure 3. (A) Coordinate system for three-di mensional vector analysis of the forces generated by the cran ial musculature of H. francisci Directionality is defined with respect to the head of H. francisci using the “right-hand rule.” (B) Schematic diagram of the jaws of H. francisci indicating variables for mechan ical lever-ratio analysis. AB, resolved in-lever for jaw adduction; AC, out-l ever; BD, resolved a dductive muscle force vector; PBOB, maximum tetanic tension. CT-scan image used with permission of A. Summers. to the point of insertion of the coracoma ndibularis was determin ed from the threedimensional coordinates. In-l evers for jaw adduction from th e center of rotation of the jaw joint to the points of insertion on the lower jaw of the quadratomandibularispreorbitalis complex, quadratomandibularis, and preorbitaliswere determined in the same manner. A weighted average of these in -levers was determined based on the forces produced by their respective muscles. The a bductive and weighted adductive in-levers were divided by the out-lever distance from th e center of rotation of the jaw joint to the tip of the anterior-most tooth of the lower jaw to determine mechanical advantage ratios for jaw opening and closing (Fig. 3B). Due to the quadratomandi bularis-preorbitalis complex’s broad surface attachment on the la teral face of both the upper and lower jaws, an exact insertion point for this muscle co uld not be identified. Its center of mass and principle muscle fiber direction relative to the lower jaw were used to approximate its mechanical line of action. The distance from the jaw joint to the intersection of this line

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10 of action with the lower jaw served as the in-lever for this muscle. Anatomical nomenclature is based on Daniel (1915), Motta and Wilga (1995, 1999), and Nobiling (1977). Theoretical Force Generation Anatomical cross-sectional area (CSA) meas urements of the nine parallel fibered muscles were multiplied by the specific tens ion of elasmobranch white muscle (289 kN/m 2 (Lou et al., 2002)) to determine their theoretical maximum tetanic forces (P O ): P O = CSA specific tension Anatomical cross-sectional area was used in th is analysis because theoretical estimates of maximum bite force based on the anatomical cr oss-sectional area of the parallel fibered jaw adducting musculatur e of the spiny dogfish Squalus acanthias best approximated bite forces measured during tetanic stimulation of the jaw adducting musculature (Huber and Motta, 2004). Force vectors for each muscle were constructed from their maximum tetanic forces and the three-dimensional coor dinates of their origin s and insertions. The force vectors of muscles exci sed unilaterally were refl ected about the Y-plane to represent the forces generated by the muscul ature on the other side of the head. Mathcad 11.1 software (Mathsoft, Inc.) wa s used to generate a three-dimensional model of the static for ces acting on the jaws of H. francisci during prey capture. Summation of the three dimensional moments acting on the lower jaw about the jaw joints (left and right) determined the theoretic al maximum bite force for each individual, and the average maximum bite force for all individuals (F B Fig. 4). Maximum bite force was modeled at points 0, 25, 50, 75, and 100% of the distance along the functional tooth

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11 Figure 4. Forces involved in the static e quilibrium calculations of the lower and upper jaws of H. francisci FBBB, bite reaction force; FBEB, reaction force at the ethmoidal articulation; FBHB, reaction force at the hyo mandibular articulation; FBJRB, jaw joint reaction force; FBPOB, force generated by the preorbitalis-BB FBQM-POB, force generated by the quadratomandibularis-pre orbitalis complex; FBQMB, force generated by the quadratomandibularis; FBRB, resultant adductive force; angle of incidence of FBEB relative to the articular surface of the upper jaw at th e ethmoidal articulation. Arrow size does not indicate force magnitude and angles of fo rce vectors are approximate. CT-scan image used with permission of A. Summers. row from the posterior-most tooth to determine a bite force gradient along the lower jaw. Additionally, the reaction force acting on the jaw joints during bites occurring at 0 and 100% of the distance along the func tional tooth row was determined (FBJRB, Fig. 4). Loadings were determined at the ethm oidal and hyomandibular articulations of the upper jaw with the chondrocranium and hyom andibula, respectively (Figs 1A, 4). For bites occurring at 0% (posterior-most mo lariform tooth) and 100% (anterior-most cuspidate tooth) of the distance along the f unctional tooth row, the moments acting on the

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12 upper jaw about the ethmoidal articulation were summed to determine the forces acting at the hyomandibular articulation (FBHB, Fig. 4). In these analyses the hyomandibula was modeled as a two-force member, moveable a bout its articulations with both the upper jaw and chondrocranium (Hibbeler, 2004). Static equilibrium analysis of the forces acting on the upper jaw was then used to determine the forces acting at the ethmoidal articulation (FBEB, Fig. 4). Static equilibrium conditions for the forces acting on the lower (FBLJB ) and upper jaws (FBUJB) were: FBLJB = FBJRB + FBQM-POB + FBQMB + FBPOB + FBB B= 0 FBUJB = FBJRB + FBHB + FBQM-POB + FBEB + FBB B= 0 where FBBB is the bite reaction fo rce from a prey item, FBEB is the force at the ethmoidal articulation, FBHB is the force at the hyo mandibular articulation, FBJRB is the jaw joint reaction force, FBPOB is the force generate d by the preorbitalis-BB FBQM-POB is the force generated by the quadratomandibularis-pre orbitalis complex, and FBQMB is the force generated by the quadratomandibularis. Forces generated by the preorbitalis-BB and quadratomandibularisare isolated to the lower jaw because they originate on the chondrocranium and insert only upon the lowe r jaw (Figs 2A, 4). Joint reaction forces maintain the static equilibrium of feedi ng mechanisms by balancing the moments acting upon the jaws via their associated musculatur e and contact with pr ey items. The moment acting on the lower jaw during jaw opening via the coracomandibularis muscle was used to determine the theoretical maximum jaw opening force of H. francisci In Situ Bite Performance Measurements Bite performance measurements were pe rformed using a modified single point load cell (Amcells Corp., Carlsbad, CA, USA) with custom designed stainless steel lever

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13 arms, which was calibrated using a seri es of known weights. Free-swimming H. francisci were trained to voluntarily bite the trans ducer by wrapping the de vice in squid and presenting it to them after several days of food deprivation. A P-3500 strain indicator (Vishay Measurements Group, Raleigh, NC, USA) was used for transducer excitation and signal conditioning. Data were acquired w ith a 6020E data acquisition board and LabVIEW 6.0 software (National Instru ments Corp., Austin, TX, USA). Fifteen measurements of bite force were taken fr om each animal. Only events in which the transducer was bitten between the tips of th eir jaws were kept for analysis. The five largest bite force measurements for each individual were analyzed for the following performance variables, as well as used in the multivariate statistical analyses described below: maximum force (N), duration of force production (ms), time to maximum force (ms), rising slope of force-time curve (N sP-1P), duration at maximum force (ms), time from maximum force to end of force production (her eafter referred to as “time away from maximum force” (ms)), falling sl ope of force-time curve (N sP-1P), and impulse ( I ), which is the integrated area under the force-time curve (kg m sP-1P) from the initiation of force generation to its cessation: I = F dt The impulse of a force is the extent to which that force changes the momentum of another body, in this case being the force transducer, and therefore has the units of momentum (kg m sP-1P). For each individual, the single larg est bite force and its associated performance measurements were used to crea te a profile of maximum bite performance for H. francisci to compare the dynamics of the as cending and descending portions of the bite performance waveforms, and to compare the maximum bite forces obtained from the

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14 theoretical, in situ restrained, and stimulated methods of determining bite force (see below). In situ bite performance measurements were simultaneously filmed with a Redlake PCI-1000 digital video system (Redlake MASD, San Diego, CA, USA) at 250 frames per second to verify that bites on the transducer occurred between the tips of the jaws (hereafter referred to as transducer bite s). The modified singl e point load cell used in this study averages the signals generated by four stra in gages in a full Wheatstone bridge such that the transducer is insensitiv e to the position on the lever arms at which the bite is applied. Therefore, the point at which a shark bit the lever arms of the transducer did not need to be determined from th e digital video sequences for appropriate calibration. To identify any behavioral artifacts associated with biting a stainless steel transducer, H. francisci were also filmed while consuming pieces of O. oglinum cut to the same size as the biting surface of the force transducer (hereafter referred to as fish bites). The following kinematic variables were quantified from transducer and fish bites using Motionscope 2.01 (Redlake MASD) and Sigma Scan Pro 4.01 (SPSS, Inc.) software: distance, duration, velocity, and acceleration of lower jaw depression, lower jaw elevation, upper jaw protrusion, and h ead depression; maximum gape; time to maximum gape; time to onset of lower jaw elev ation; time to onset of head depression; cranial elevation angle. All kinematic variables were quant ified using discrete cranial landmarks as reference points (Edmonds et al., 2001). Restrained and Stimulated B ite Performance Measurements At least one week after the in situ bite performance measurements, four of the previous H. francisci were individually removed from the experimental tank and

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15 restrained on a table. Once they had opene d their jaws an adequate distance, the transducer was placed between the anterior teeth, which elicited an aggressive bite. Following a recovery period of approxima tely 10-15 minutes, the shark was again removed from the tank and anaesthet ized with MS-222 (0.133 g/l). The quadratomandibularis-preorbitalis complex, quadratomandibularis, and preorbitaliswere implanted with stainless steel 23 gauge hypodermic needles connected to a SD9 stimulator (Grass Telefactor, West Warwic k, RI, USA) and tetanic fusion of these muscles was accomplished via stimulati on (10V, 100 Hz, 0.02 ms delay, 3ms pulse width) while the bite force transducer was pl aced between the tips of the anterior teeth. Three measurements were taken from each individual in both of these experimental protocols. Individuals were ventilated with aerated seaw ater between measurements during muscle stimulation experiments. Maxi mum bite force, time to maximum force, and time away from maximum force were quant ified from all restrained and stimulated bites. Statistical Analysis All bite performance and kinematic variables were LogB10B transformed and linearly regressed against body mass to remove the eff ects of size. Studentized residuals were saved from each regression for subsequent analysis (Quinn and Keough, 2002). Principal components analyses (PCA) based on correlation matrices were then used to 1) identify covariation in bite performa nce variables and reduce these variables to a series of noncorrelated principal components, which were su bsequently analyzed to assess the extent of individual variability in these parameters; 2) identify covariation in performance and kinematic variables from in situ bite performance trials; and 3) identify covariation in

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16 kinematic variables from fish and transducer bites and reduce these variables to a series of non-correlated principal component s, which were subsequently analyzed to determine whether there were any behavioral artifacts associated with biting the steel transducer. Variables were considered to load strongly on a given principal component (PC) if their factor scores were greater than 0.6. Non-rotated axes described the greatest amount of variability in each PC A. For analyses 1 and 3, multiv ariate analysis of variance (MANOVA) was used to compare the factor scores for the PCs with eigenvalues greater than 1.0. To determine whether fish and transducer bites kinematically differed, a two-way, mixed-model MANOVA was perf ormed on the PCs from PCA 3 with individual as the random effect and prey type as the fixed effect, which was tested over the interaction mean square. Kinematic data from four indivi duals were included in this analysis because a complete data set was l acking for one individual. To determine the extent of individual variability within th e bite performance variables, a one-way MANOVA was performed on the PCs from PCA 1. To determine whether the kinematic va riables associated with biting the transducer were predictive of biting performance in H. francisci stepwise (forward) multiple regressions were performed with kinematic variables measured from transducer bites as the multiple independent factors, and the eight bite performance variables as the individual dependent factors. Data from four individuals were included in this analysis because a complete kinematic data set was lacking for one individual. One-way ANOVA on studentized residuals was used to identify significant differences among the theoretical, in situ restrained, and electrically stimulated methods of determining maximum bite force. A Student's t-test was used to identify differences between time to

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17 maximum force and time away from maximum force, and the rising and falling slopes of the force-time curves for in situ biting trials. One-way ANOVA was used to compare time to maximum force and time away from maximum force within and among in situ restrained, and electrically stimulated bite fo rces. Lastly, bite forces at the anterior jaw (fish, reptiles, and birds) or canine te eth (mammals) and body masses for various vertebrates were compiled from the availabl e literature and grouped according to major taxonomic level. These bite forces, along with those of the horn sharks investigated in this study, were linearly regressed against body mass. Studentized residuals from this regression were then coded according to taxonomic level and compared with a one-way ANOVA. All significant differe nces were investigated post-hoc with Tukeys pairwise comparisons test. Linear regressions were performed in SigmaStat 2.03 (SPSS Inc.) in order to obtain studentized re siduals. All other statistical analyses were performed in SYSTAT 10 (SPSS, Inc.) with a p-value of 0.05. Results Biomechanical Modeling The quadratomandibularis-preorbitalis complex, which is the primary jaw adductor, generated the greatest force of all muscles investigat ed (242 N, Table 1). Of the muscles active during jaw and hyobranchial a bduction, the coracobr anchiales generated the greatest force (107 N, Table 1). The levator hyomandibularis generated more force during the retractive phase (33 N) than the le vator palatoquadrati (20 N, Table 1). After resolving the force generated by the adductor musculature into its principal components, the majority of force was directed dorsally (294 N) and anteriorly (128 N). The Z-axis

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18 Table 1. Theoretical maximum forces generate d by the cranial musc ulature active during the gape cycle in H. francisci Action Muscle Theoretical Max Force (N)P §P Coracomandibularis 31 +/5 Coracohyoideus 57 +/4 Coracoarcualis 87 +/4* Jaw & Hyobranchial Abduction Coracobranchiales 107 +/8* Quadratomandibularis44 +/2* Preorbitalis52 +/5* Jaw Adduction QM-PO Complex 242 +/11* Levator Palatoquadrati 20 +/1* Jaw & Hyobranchial Retraction Levator Hyomandibularis33 +/1* § mean +/S.E. bilateral muscle force for paired muscles component of this force (19 N per side) were di rected laterally on eith er side of the head, and negate each other during jaw adduction (Table 2, Fig. 3A). Thus, the resultant adductive force along the z-axis was 0 N. The large anterodorsally directed component of this adductive bite force (FBRB, Fig. 4) drives the lower jaw towards the upper jaw, which is itself driven into the ethmoid region of the chondrocranium (FBEB, Fig. 4). Summation of the moments acting on the lower jaw determined that the maximum theoretical bite force of H. francisci ranged from 128 N at the an terior teeth to 338 N at the posterior-most molariform teeth (Fig 5, Ta ble 2). The bite force at the posterior-most molariform teeth exceeded the resultant fo rce generated by the adductive musculature (Table 2) because the mechan ical advantage at this poi nt along the jaw was 1.06. The resultant jaw closing mechanical advantage at the anterior teeth was 0.51, re sulting in a dramatically lower bite force at this point.

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Table 2. Resultant bilateral muscle and jaw forces occurring during prey capture in H. francisci broken into their principal components Variable Resultant Force (N) F X (N) F Y (N) F Z (N) Resultant Abductive Muscle Force 31 25 -19* 0 Resultant Adductive Muscle Force 321 -128* 294 0 Opening Force a 16 0 -16* 0 Biting Force a (F B ) 128 0 128 0 Biting Force b (F B ) 338 0 338 0 negative values indicate forces acting in the negative direction on their respective axes (see Fig. 3A) a, force at the tips of the jaws; b, force at the back of the jaws Figure 5. Theoretical maximum bite force (N) of five male H. francisci (n = 5, TL = 55-68 cm) from three-dimensional vector analysis of the jaw adducting musculature measured at 0, 25, 50, 75, and 100% of the length of the functional tooth row of the lower jaw from posterior to anterior. CT-scan image used with permission of A. Summers. 19

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20 Table 3. Unilateral mechanical loadings at articulation points in the feeding mechanism of H. francisci broken into their principal components Variable Resultant Force (N)FBX B(N) FBY B(N) FBZ B(N) Joint Reaction ForcePaP (FBJRB) 106 69 -80* 0 Joint Reaction ForcePbP (FBJRB) 73 69 25 0 Loading at Ethmoidal Artic.PaP (FBEB) 59 10 -59* 0 Loading at Ethmoidal Artic.PbP (FBEB) 59 10 -59* 0 Loading at Hyomandibular Artic.PaP (FBHB)36 10 22 27 Loading at Hyomandibular Artic.PbP (FBHB)36 10 22 27 negative values indicate forces acting in the negative direction on their respective axes relative to the right side of H. francisci’s head (see Fig. 3A) a, force at the tips of the jaws; b, force at the back of the jaws The jaw joint reaction forces (FBJRB, Fig. 4) occurring when prey is captured at the anterior teeth and crushed at the posterior teeth by H. francisci were 106 N and 73 N per side, respectively (Table 3). This force wa s oriented posteroventrally relative to the articular surface of the lower jaw joint for anterior biting, and consequently oriented anterodorsally relative to the articular surf ace of the upper jaw joint. The local/internal loadings on the joint between the upper and lower jaws indicate that the jaw joint is globally in compression (Hibbeler, 2004) when prey is bitten at the tips of the jaws. When prey is crushed between the posterio r molariform teeth the orientation of the vertical component of the jo int reaction force relative to the lower jaw (25 N) was opposite that for the lower jaw joint dur ing anterior biting (-80 N), indicating tensile loading of the jaw joint during pos terior prey capture (Table 3). The ethmoidal articulation of H. francisci received a loading of 59 N per side during biting, regardless of whet her biting occurred at the ante rior or posterior margin of the jaws (FBEB, Fig. 4). The angle of incidence of this force relative to the articular surface of the upper jaw at the et hmoidal articulation was 80 ( Fig. 4). For both anterior and

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21 posterior biting, the majority of loading wa s directed ventrally into the upper jaw, indicating compression between the ethmoid region of the chondrocranium and the palatal region of the upper jaw (Table 3). The magnitude of loading at the hyo mandibular articulation (36 N) was independent of bite point as well (FBHB, Fig. 4). The lower jaw was loaded posterodorsally and medially at its articulation with the hyom andibula during both anterior and posterior biting (Table 3). The reaction forces acting on the distal ends of the hyomandibula are equal to and opposite the forces acting at the jaws’ articulation with the hyomandibula. Therefore, during biting the hyomandibula wa s loaded anterovent rally and laterally. These local/internal loadings between th e jaws and hyomandibula indicate that the hyomandibula is globally in tension Modeling the hyomandibula as a two-force member assumed that the line of action of the for ce acting on the hyomandibula passed through its articulation with the jaws and chondrocranium The hyomandibula is therefore loaded in pure tension and the angle of incidence of th e hyomandibular force cannot be determined. The only muscle involved in abduction of the lower jaw is the coracomandibularis, which was capable of ge nerating 31 N of force (Table 1). This muscle inserts on the caudal aspect of the lower jaw symphysis at 37 below the longitudinal axis of this jaw, and has a m echanical advantage of 0.89. Despite this high mechanical advantage, indicative of force am plification in a class III lever system, its acute insertion angle caused the muscular force generating motion about the lower jaw (force component perpendicular to the lower jaw) to be 19 N (Table 2). After accounting for mechanical advantage, the resultant abducti ve force at the tip of the lower jaw was 16 N (Table 2). The abductive force lacks a component along the Z-axis because the

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22 coracomandibularis runs parall el to the longitudinal axis of the body. The other muscles involved in the expansive phase of the gape cycle generated considerably greater forces than the coracomandibularis (Table 1). Performance Measurements In situ measurements : H. francisci approached and bit the force transducer in an attempt to remove the attached food. In mo st cases biting continued until the food was removed from the transducer. PCA 1 reduced the performance variables for each individual to three PCs (89.7% of varian ce explained), each of which indicated considerable overlap among individuals. MANOVA subsequently demonstrated no differences among individuals fo r bite performance variables using size-corrected data (Wilks Lambda = 0.51, F 12,47 = 1.157, p = 0.340). The average maximum in situ bite force measured at the anterior teeth was 95 N, with an absolute maximum force of 133 N (66 cm male H. francisci). Heterodontus francisci took approximately 322 ms to reach maximum bite force, which was held for 41 ms, and released after an additional 212 ms (Table 4). The average duration of force ap plication was 535 ms. Time to maximum bite force was longer than the time away from maximum bite force ( p = 0.049). The mean rising slope of the force-time curve was 300 N s -1 and was lower than the average falling slope of 457 N s -1 ( p = 0.048). The average impulse generated from the beginning of force application until its cessation was 25 kg m s -1 but measured as high as 44 kg m s -1 The majority of bite force waveforms consisted of single peaks associated with single bites. However, in 32% of the bites multip le peaks occurred indicating a repetitive crushing behavior during fo rce application (Fig. 6).

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Table 4. In situ bite performance data for H. francisci biting at the tips of its jaws Variable Minimum Maximum Mean +/S.E. Maximum Force (N) 60 133 95 +/13 Force Duration (ms) 400 721 535 +/60 Time to Maximum Force (ms) 241 428 322 +/33 Time at Maximum Force (ms) 31 55 41 +/4 Time away from Maximum Force (ms) 146 303 212 +/35 Impulse (kg m s -1 ) 11 44 25 +/6 Rising Slope of Force-Time Curve (N s -1 ) 200 400 300 +/34 Falling Slope of Force-Time Curve (N s -1 ) 305 696 457 +/65 Figure 6. Bite force waveforms from bite performance trials of three male H. francisci (TL = 66-70 cm) illustrating in situ voluntary bites with single (black) and double (light gray) force peaks, and a bite from a restrained individual (dark gray). 23

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24 PCA 2 of performance and kinematic vari ables yielded 6 PCs with eigenvalues greater than 1.0, which collectively explained 86.7% of the va riance. All of the variables that loaded heavily on the first PC (30.5% of variance explained) were kinematic measurements (Table 5). These variables pr imarily demonstrated covariance in the timings and excursions of lower jaw depression and elevation. Performance measures were the only variables to load heavily on the second PC (19.5% of variance explained), indicating covariance between rates and durations of forc e application (Table 5). Maximum bite force did not load heavily until the fifth PC (7.8% of variance explained) and impulse did not load heavily on any of the PCs. Stepwise multiple regressions yielded si milar results to PCA 2 on kinematic and performance data. Only three of the bite performance variables were significantly related to individual kinematic variables. Force dur ation was significantl y, though poorly, related to lower jaw elevation velocity (R 2 = 0.226, F 1,18 = 5.268, p = 0.034). Similarly, time to maximum force (R 2 = 0.389, F 1,18 = 11.471, p = 0.003) and the rising slope of the force time curve (R 2 = 0.410, F 1,18 = 12.523, p = 0.002) were significantl y related to lower jaw elevation distance. Inclusi on of additional kinematic va riables did not improve the predictive ability of these regression models. The two va riables indicative of the magnitude of bite force generated (maximum force, impulse) could not accurately be predicted by any combination of kinematic variables. Although kinematic variables were not predictive of bite performance variables, PCA 1 used to assess individual variability (see above) identified notable covarian ce in performance measures. Maximum in situ bite force exhibited a strong linear relationship with impulse (R 2 = 0.758), and moderate

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25 Table 5. Principal component lo adings of performance and kinematic variables from bite performance trials of H. francisci Variable PC 1 PC 2 Lower Jaw Depression Distance 0.718* 0.179 Lower Jaw Depression Duration 0.820* 0.066 Lower Jaw Depression Velocity 0.122 0.183 Lower Jaw Depression Acceleration -0.378 0.199 Time to Maximum Gape 0.741* 0.182 Maximum Gape 0.496 0.467 Head Angle 0.403 0.334 Onset of Lower Jaw Elevation 0.830* 0.015 Lower Jaw Elevation Distance 0.727* 0.219 Lower Jaw Elevation Duration 0.459 0.530 Lower Jaw Elevation Velocity -0.533 0.352 Lower Jaw Elevation Acceleration -0.710* -0.001 Time to Lower Jaw Elevation 0.939* 0.098 Time to Maximum Force -0.051 -0.772* Time at Maximum Force 0.325 -0.704* Time Away from Maximum Force 0.593 -0.475 Force Duration 0.326 -0.829* Rising Slope 0.152 0.800* Falling Slope -0.457 0.643* Impulse 0.460 -0.127 Maximum Force 0.069 0.305 bold values indicate variables c onsidered to load heavily on a given principal component (loading score > 0.600)

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Figure 7. Maximum in situ bite force (N) from five male H. francisci (n = 5, TL = 63-74 cm) plotted against (A) impulse (kg m s -1 ) and (B) force duration (ms) on logarithmic axes. 26

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27 linear relationships with force duration (R 2 = 0.450) and time to maximum force (R 2 = 0.489) (Fig. 7). PCA 3 reduced the set of kinematic variab les measured from fish and transducer bites to a series of four PCs (73.3% of variance explained). MANOVA indicated no significant differences between the prey capture kinematics of H. francisci while bitingfish or the transducer on any of the PC s for all individuals (Wilks Lambda = 1.0, F 4,29 = 0.0, p = 1.0). However, a single individual was found to differ from two other individuals on the first PC (F 3,32 = 4.646, p = 0.008). Variables that loaded heavily on the first PC were durations and distances of lower jaw depre ssion and elevation, times to maximum gape, onset of lower jaw elevation, and completion of lower jaw elevation, and maximum gape distance. The acceleration of lower jaw elevation loaded heavily, but negatively on the first PC. Methodological Comparison In situ measurement of maximum bite for ce was a reasonably good indicator of the maximum bite force of H. francisci Using size-corrected da ta, a single difference was found among the four methods of determining maximum bite force (F 3,14 = 4.358, p = 0.023). Restrained bite force (159-206 N) was significantly greater than in situ bite force (60-133 N) ( p = 0.013). In situ bite force was, however, e quivalent to theoretical (107163 N) and electrically stimulated (62-189 N) bite forces. Restrained, electrically stimulated, and theoretical bite forces were e quivalent (Table 6). Du ring restrained bites, time to maximum force (522 ms) was greater than time away from maximum force (339 ms) (t 4 = 2.848, p = 0.046). Time to maximum force (285 ms) was shorter than time away from maximum force (556 ms) for electrically stimulated bites (t 8 = -5.476, p < 0.001).

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28 Table 6. Results of one-way ANOVA on different methods of determining bite force at the tips of the jaws in H. francisci in situ Theoretical Stimulated Restrained **Avg. Max. +/S.E. (N) 95 +/13 128 +/10 132 +/24 187 +/14 *Statistically similar values are underlined **Average of the single largest bite force values from each individual Significant differences were detected between the in situ restrained, a nd electrically stimulated methods for time to maximum force (F 2,10 = 4.996, p = 0.031) and time away from maximum force (F 2,10 = 58.290, p < 0.001). Time to maximum force was greater for restrained bites than elect rically stimulated bites ( p = 0.030), both of which were equivalent to the time to maximum force of in situ bites. Time away from maximum force was greater for electrically stimu lated bites than restrained bites ( p = 0.001), which was greater than that of in situ bites ( p = 0.005). Bite Forces Among Vertebrates Bite forces and body masses were co mpiled for 113 species of vertebrates (including H. francisci ) from the available literature (Ringqvist, 1972; Robins, 1977; Thomason et al., 1990; Cleuren et al., 1995; Hernandez and Motta, 1997; Clifton and Motta, 1998; Herrel et al., 1999, 2001, 2002; Binder and Van Valkenburgh, 2000; Thompson et al., 2003; Erickson et al., 2004; Huber and Motta, 2004; Korff and Wainwright, 2004; van der Meij and Bout, 2004; Wroe et al ., 2005; Huber et al., 2006, in prep) (Appendix I). Collectively, bite force scaled to body mass with a coefficient of 0.60, which is below the isometric scaling coefficient of 0.67 (Fig. 8). When the mammalian bite forces from Wroe et al. (2005) were excluded from this analysis bite

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29 Figure 8. (A) Bite forces (N) of various vertebrates plotted ag ainst mass (g). (B) Residuals from regressi on analysis of LogB10B bite force versus LogB10B mass plotted against LogB10B mass (g). Dashed lines indicate 1 standard deviation about the residual mean.

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30 force scaled with a coefficient of 0.66, appr oximating isometry. This discrepancy is likely due to Wroe et al. (2005) having used the dry-skull method of estimating muscle CSA, which can underestimate CSA by 1.3-1.5X (Thomason et al., 1991). Fishes collectively had the highest mass spec ific bite force of the four vertebrate groups, followed by reptiles, mamm als, and birds respectively (FB3,130B = 6.357, p < 0.001). Mass specific bite force of the fishes was greater than those of the birds ( p = 0.002) and mammals ( p = 0.013), while reptilian mass specific bite force was greater than that of the birds ( p = 0.009). The striped burrfish Chilomycterus schoepfi had the highest mass specific bite force, followed by the Canary Island lizard Gallottia galloti and the American alligator Alligator mississipiensis (Herrel et al., 1999; Erickson et al., 2004; Korff and Wainwright, 2004). The hogfish Lachnolaimus maximus had the second highest mass specific bite force, but for biting with the pharyngeal jaws, not the oral jaws (Clifton and Motta, 1998). The th ree lowest mass specific bite forces were those of the red-bellied shortnecked turtle Emydura subglobosa mata mata turtle Chelus fimbriatus and twist-necked turtle Platemys platycephala (Herrel et al., 2002) (Fig. 8). Of the cartilaginous fishes in this analysis, the mean mass specific bite force of H. francisci was greater than those of S. acanthias and the blacktip shark Carcharhinus limbatus but less than that of the white-spotted ratfish Hydrolagus colliei Discussion Functional Morphology The jaw adducting cranial musculature (QM-PO complex, QM, POon Fig. 2) of H. francisci generates more force during prey capture than either the jaw and

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31 hyobranchial abducting or retracting musculature. The mechanical advantage of H. francisci s jaw adducting mechanisms ranges from 0.51 at the tip of the jaws to 1.06 at the posterior margin of the f unctional tooth row. In class II I lever systems such as shark jaws, a mechanical advantage greater than 1.0 indicates that the point at which force is being applied to a prey item is closer to the jaw joint than the point at which muscular force is being applied to the jaw, resulting in an amplification of the muscular force. Subsequently, the theoretical maximum bite force at the posterior margin of the functional tooth row exceeds the resultant force generated by H. franciscis adductor musculature. This amplification of muscular force is advantageous for the processing of hard prey such as the molluscs, echinoderms, and benthic crustaceans consumed by H. francisci (Strong Jr., 1989; Segura-Za rzosa et al., 1997). The jaw closing mechanical advantage at the anterior teeth of H. francisci is greater than that of the only other elasmobr anch for which values have been published, S. acanthias (0.28 (Huber and Motta, 2004)), which utilizes a combination of ram and suction feeding to consume soft-bodied prey (Wilga and Motta, 1998a). Its jaw closing mechanical advantage is greater than thos e at the anterior teeth of nearly every actinopterygian fish investigated (~150), which include prey from plankton to hardshelled species (Turingan et al., 1995; Durie and Turingan, 2001; Wainwright et al., 2004; Westneat, 2004). The durophagous species among these taxa do, however, have the highest jaw adducting mechanical advantages The durophagous parrot fishes (Scaridae) are the only actinopterygian fishes with jaw adducting mechanical advantages comparable to that of H. francisci (Wainwright et al., 2004; We stneat, 2004). Thus, there

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32 is extensive evolutionary convergence on high leverage jaw adducting mechanisms in fishes that consume hard prey. The jaws of H. francisci are elliptical in tr ansverse-section, with their major axis oriented vertically, in-line w ith the compressive stresses associated with feeding. Calcium reinforcement in the jaw cortex increases posteriorly as the dentition becomes more molariform, and is greatest at the jaw join ts (Summers et al., 2004). Calcification and elliptical geometry increase the second moment of area of the jaws with respect to the compressive loading of prey capture and pro cessing, which augments the jaws ability to resist dorsoventral flexion (Summers et al ., 2004). The resolved force vector for jaw adduction also occurs approximately in the regi on of the most robust molariform teeth of H. francisci where it can generate upwards of 338 N of bite force. Therefore, maximum bite force is produced where bot h the dentition and ja w cartilages are best able to resist compressive stresses. Despite the high mechanical advantage ( 0.89) of the coracomandibularis muscle in the lower jaw depression mechanism of H. francisci its acute insertion angle relative to the lower jaw causes most of its force to be directed posteriorly, into the jaw joints (Table 2.) This high mechanical advantage is due the insertion of the coracomandibularis on the posterior margin of the mandibular symphysis, which is synapomorphic for chondrichthyans (Wilga et al., 2000). Although this mechanism is suited for force production, velocity production is desi rable for inertial suction feeding. Heterodontus francisci nonetheless effectively us es suction to initially cap ture and reorient prey (Edmonds et al., 2001), which may be due in part to its powerful hyoid and branchial abductors (Table 1). These muscles rapidl y expand the floor of the buccopharyngeal

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33 cavity, which is critical to suction feed ing in elasmobranchs (Motta et al., 2002; Svanback et al., 2002). As in the nurse shark Ginglymostoma cirratum (Motta et al., 2002), the large labial cartilages of H. francisci considerably occlude its lateral gape, theoretically augmenting su ction ability (Muller and Osse, 1984; Van Leeuwen and Muller, 1984). Three-dimensional resolution of the fo rces generated during jaw adduction may reveal the mechanical basi s of upper jaw protrusion in H. francisci The force driving the upper jaw into the ethmoidal articulation has both dorsal and anterior components, causing the upper jaw to slide th rough the anteroventrally sl oping palatal fossa of the chondrocranium and protrude (Fig. 4, Table 2). This proposed mechanism is based on the resolved force vector for all muscles invol ved in jaw adduction. Differential activity of the heads of this complex may fac ilitate modulation of protrusion. The quadratomandibularisis the likely candidate for c ontrol over protrusion because its acute insertion angle relative to the lower ja w and anterior inserti on point give it high leverage over anterior motion (Fig. 2). Activity of the quadratomandibularis-pre orbitalis complex alone, which has a broad insertion on the lateral face of both the upper and lower jaws, may contribute to protrusion of the upper jaw as well. After th e lower jaw has been depressed, contraction of this muscle complex may simultaneously raise the lower jaw and pull the upper jaw away from the skull. This mechanism has been proposed for upper jaw protrusion in S. acanthias G. cirratum and the lemon shark Negaprion brevirostris (Moss, 1977; Motta et al., 1997; Wilga and Motta, 1998a). Protrusion by H. francisci which may be used to chisel away at attached benthic prey, occu rs after the lower ja w has been depressed

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34 (Edmonds et al., 2001), corroborating the role of the quadratomandi bularis-preorbitalis complex in this behavior. Extensive calcification near the jaw joints of H. francisci (Summers et al., 2004) would apparently indicate hi gh joint reaction forces during prey capture. Joint reaction forces can exceed bite forces at the tip of the jaw depending on the mechanical advantage of the given feeding mechanism and the for ce produced by the associated musculature, which has been identified in numerous reptiles (3-4 times gr eater) (Cleuren et al., 1995; Herrel et al., 1998). Although join t reaction force was greater th an anterior bite force in H. francisci the ratio of these values (1.65) is substantially lower than those found for reptiles. The ratio of joint reaction force to posterior bite force in H. francisci was 0.43. Low ratios of joint reaction force to bite force in H. francisci are due to its high mechanical advantage jaw adducting m echanism. Humans, which share this characteristic, have correspondingly low ratios of joint reaction force to bite force (Koolstra et al., 1988). Although some damping will occur in the connective tissue associated with the jaw joint, loading occurring at the joint will be transmitted to adjacent skeletal elements. Therefore, low ratios of joint reaction force to bite force may be adaptive in H. francisci and elasmobranchs in general, because the posterior region of their jaws is suspended from the cranium by mobile hyomandibulae, not a stable jaw articulation as in other vertebrates. Minimizi ng loading at this articulation may stabilize the feeding mechanism during pr ey capture and processing. In heterodontiform sharks, the cranial stresses associated with prey capture can be isolated to the ethmoidal and hyomandibular articulations. Unlike carcharhinid sharks (Motta and Wilga, 1995), the upper jaw of H. francisci does not disarticulate from the

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35 chondrocranium during feeding, even dur ing upper jaw protrusion (Maisey, 1980). Therefore, in carcharhinid sharks the hyoma ndibulae may receive all of the suspensorial loading occurring during prey capture. Optim al loading at the ethmoidal articulation would entail forces directed perpendicularl y into the articular surface of the upper jaw because cartilage is strongest in axia l compression (Carter and Wong, 2003). The estimated forces at this articulation devi ated from optimal orientation by only 10 during anterior and posterior biting. The ethmoidal articulation of H. francisci appears well designed for withstanding this nearly axia l compressive loading because the upper jaw calcifies at this articulati on early in ontogeny (Summers et al., 2004) and the ethmoid region of the chondrocranium is one of the thic kest parts of this st ructure (Daniel, 1915). Additionally, maintenance of contact between the upper jaw and chondrocranium in H. francisci will distribute stresses from the repeti tive loading associated with processing hard prey. Although it is well known that the hyomandi bulae support the posterior margin of the jaws, the nature of the lo ading they receive has been a matter of speculation. This mechanical analysis indicat es that the hyomandibulae of H. francisci are tensile elements as suggested by Moss (1972) and Frazzetta (1994). Consequently, the hyomandibulae may regulate anterior movement of the jaws during feeding, such as would occur during jaw protrusion. In this regulatory role, act ivity of the levator hyomandibularis could hypothetically modulate resistance to anteri or motion of the jaws. Electromyographic analysis of the feeding musculature of H. francisci would be required to verify this hypothesis.

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36 The ligamentous attachments between the hyoid arch and the posterior end of the jaws stabilize this articulation against the te nsile stresses caused by biting. The internal hyomandibular palatoquadrate and hyoideo-mandibulare ligaments resist dorsoventral translation between the hyomandibula a nd jaws, while the hyomandibuloceratohyal ligament prevents lateral translation between these elements. The two slips of the median ligament (Daniel, 1915) stabiliz e against dorsoventral and late ral translati on respectively. Although this analysis makes the assumption that the hyomandibulae are loaded as twoforce members in axial tension, they likely e xperience a more diverse loading pattern in nature, necessitating this multidirectional support. Increased hyomandibular loading may have played a role in the transition from amphistylic to hyostylic jaw suspensions in modern elasmobranchs. As the number and size of the articulations between the jaws and chondrocranium was reduced, the hyomandibulae took on a greater role in susp ending the jaws (Schaeffer, 1967; Maisey, 1980; Carroll, 1988). Concomitant with these changes in articulation, the hyomandibulae became shorter and more mobile (Schaeffer, 1967; Moy-Thomas and Miles, 1971; Maisey, 1985; Cappetta, 1987), oriented more orthogonally to the chondrocranium (Stahl, 1988; Wilga, 2002), and had more extensive lig amentous attachments with the jaws and chondrocranium (Gadow, 1888). Collectively, th ese changes may have been associated with a shifting of the force of jaw adduction to a more posterior region of the jaws. This may have resulted in greater hyomandibular lo ading as well as a freeing-up of the anterior margin of the jaws such that uppe r jaw kinesis was incr eased, facilitating jaw protrusion and prey gouging (Moss, 1977; Maisey, 1980; Wilga, 2002).

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37 Although the jaw suspension mechanism of H. francisci is classified as hyostylic (Gregory, 1904; Wilga, 2002), this analysis i ndicates that it is functionally amphistylic. Heterodontus francisci exhibits considerable upper ja w kinesis (reduces maximum gape by 39%), similar to other hyostylic carcharh iniform sharks (Edmonds et al., 2001; Wilga et al., 2001). Despite this f unctional similarity, the upper ja w does not disarticulate from the chondrocranium during protrusion in H. francisci Furthermore, in contrast to the hypotheses regarding hyomandibul ar evolution (see above), H. francisci has considerable loading at both the hyomandibular (tensile) and ethmoidal (compressive) articulations. The term hyostyly should therefore be re served for taxa in which the upper jaw disarticulates from the chondrocranium dur ing protrusion such that hyomandibulae are the primary means of support, and the ethm opalatine ligaments are loaded in tension. Therefore, contemporary definitions of jaw suspension should incorporate functional interpretations of loadings at the various articulations betw een the jaws and cranium, as well as the relationship between susp ension type and upper jaw protrusion. Methodological Comparison Although no differences were found betw een theoretical, restrained, and electrically stimulated bite force measuremen ts using size corrected data, the absolute maximum bite force for each individual occurred during restrained bite force measurements. No differences were found betwee n theoretical and electrically stimulated bite force measurements of S. acanthias either (Huber and Mo tta, 2004). Therefore, restrained measurements app ear to be the best method of obtaining maximum bite force measurements from live elasmobranchs. Small sample size might, however, account for the lack of statistical sign ificance found between different methods of determining bite

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38 force. Nonetheless, the results of both this analysis and that of bite force production in S. acanthias (Huber and Motta, 2004) indicat e that theoretical estima tes of bite force in sharks are accurate in predicting maximum bite forces. This is fortunate given the logistical problems associated with obtai ning bite force measurements from live elasmobranchs. Given the appropriate res ources, however, maximum bite force can be obtained through in situ methods as indicated by the equivalence of theoretical, electrically stimulated, and in situ bite forces in this study. In situ measurements enable the quantification of biting dynamics as well, which is informative regarding feeding performance and ecology (see below). Static estimates of force production based on muscle architecture may underestimate actual force production because active stretching of the jaw adductors during the expansive phase of the gape cycle can increase force production (Askew and Marsh, 1997; Josephson, 1999). Furthermore, by modeling the primary jaw adductor as the quadratomandibularis-preorbitalis complex instead of delineating the individual heads of this complex, variations in muscle architec ture of these heads such as pinnate insertion points may have been overlooked. If this were the case, a theoretical model of force production based on morphological cross-s ectional area alone could underestimate maximum force production. The ratios of time to and away from maximum force for in situ (1.52) and restrained (1.54) bites suggest that the appli cation of bite force by H. francisci takes longer than its release. However, the opposite relationship for these variables occurred during electrically stimulated bites. The rati o of time to and away from maximum force during electrically stimulated biting (0.51) approximates th e ratio of time for twitch

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39 tension development to relaxation (0.42) fo r pectoral fin muscle of the cuckoo ray Raja naevus (Johnston, 1980). This suggests that force generation during voluntary or stimulated biting is a function of the rate at which the adductor muscles reach tetanic fusion. Gradual summation of motor unit recr uitment during voluntary biting results in a prolonged time to maximum force, whereas ma nual, high-frequency el ectrical stimulation of the adductor muscles causes more rapid te tani and subsequently shorter times to maximum force. Time away from maxi mum force was longer for restrained measurements than in situ measurements perhaps indicating motivational differences between these two presentation methods. Feeding Performance Several bite performance va riables demonstrated patterns consistent with the durophagous diet of H. francisci The time to maximum bite force application by H. francisci was longer than time away from maximu m force, the rising slope of the forcetime curve was lower than the falling sl ope, and maximum bite force was positively related to the time to maximum force. These performance characteristic s indicate that the application of bite force is a slower, more deliberate action than its release by H. francisci Linear relationships of maximum bite force with impulse and force duration further indicate that higher bite forces are associated with slower, more deliberate closing of the jaws by H. francisci (Fig. 7). The impulse generated upon impact be tween two bodies is a measure of momentum transfer, and can be interpreted as the effort that each body exerts on the other (Nauwelaerts and Aerts, 2003). Because momentum is conserved during impact, larger impulses generated during biting transfer greater quantities of kinetic energy from

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40 the jaws to the prey. Optimizing impulse by maximizing bite force output per unit time will increase the amount of energy contributi ng to the rupture/fracture of a prey item. Heterodontus francisci capitalizes upon this when consum ing hard prey with composite exoskeletons. Sustained loading after a high-velocity initial impact is effective at fracturing composite structures such as sea urchin exoskeleto ns (calcite ossicles linked by collagenous ligaments) because composites ha rden to a saturation point upon initial compression, after which crack nucleation occurs, followed by structural failure (Provan and Zhai, 1985; Christoforou et al., 1989; Strong Jr., 1989; Elle rs et al., 1998). The prevalence of multiple force peaks within a compressive waveform of a single bite (32% of in situ bites) also indicates H. franciscis behavioral specialization for exploiting hard prey (Fig. 6). This behavi or maximizes the damage inflicted upon prey items during a given bite by ramping up the applied force multiple times, especially when there are multiple bites during a feeding event. The rate at which the strength of a composite structure degrades is a power func tion of both the strain rate and number of strain cycles (Hwang and Han, 1989). Multiple force peaks within a given bite indicate that H. francisci may have evolved motor patterns specialized for durophagy as well. High-frequency bursts of electri cal activity associated with rhythmic compression of prey items occur in the jaw adducto r musculature of the lungfish Lepidosiren paradoxa (Bemis and Lauder, 1986). Prolonged jaw adductor activity occurs in the queen triggerfish Balistes vetula (Turingan and Wainwright 1993) and bonnethead shark Sphyrna tiburo which also uses repeated compre ssions of the jaws to process prey (Wilga and Motta, 2000). All of these fish incl ude hard prey in thei r diets (Turingan and Wainwright, 1993; Wilga and Motta, 2000; Be rra, 2001). These behavioral attributes

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41 demonstrate that the way in which force is applied to prey items, and not just the magnitude of force, is likely a determinant of feeding success. Although covariation in seve ral performance measures appears related to the consumption of hard prey by H. francisci covariation was lacking between kinematic and performance variables from the in situ bite performance trials. Both principal components and multiple regression analyses demonstrated the inability of kinematic measures to predict bite performance measur es with any accuracy (Table 5). These findings beg the question, how are two series of sequential behaviors so unrelated? One would assume that at least the kinematics of lower jaw el evation (e.g. velocity, acceleration) would be predictive of biting performance (e.g. maximum fo rce, impulse). This lack of covariation is likely due to the instantaneous po sition of the jaw adducting muscles of H. francisci on the force-velocity curve relating muscle te nsion to contraction velocity (Aidley, 1998). Based on this principle, when the adductor mu sculature is elevating the lower jaw, it is contracting with high velocity and low force. However, on ce contact is made with the bite force transducer, movement of the lower jaw is impeded and the jaw adductors shift to the low velocity, high for ce region of the force-velocity curve. In addition to high force, maximum muscle power is generated at low velocity as well (Askew and Marsh, 1997). Because of the dramatic differences in mu scle function at either end of the forcevelocity curve, jaw kinematics and biting pe rformance may vary c onversely and possibly be modulated independently. A predictive re lationship between cranial kinesis and performance kinetics is more likely to be f ound for behaviors such as suction feeding in which kinesis and performance occur simulta neously (cranial expansion and suction

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42 generation) (Sanford and Wainwright, 2002; Sva nback et al., 2002), not sequentially as is the case in biting performan ce (jaw adduction and bite force application). An additional behavior that may augment the biting performance of H. francisci is the use of upper jaw protrusion to dislodge and chisel away at hard prey, as was suggested by Edmonds et al. (2001). While the restrained bite force measurements of H. francisci indicate that they can consume prey capable of resisting over 200 N using this behavior, in situ bite force measurements suggest they would consume smaller, less durable prey. An analysis of the forces necessa ry to crush various sizes of hard prey items found in H. francisci s diet is needed to delineate the pr ey it is theoretically capable of consuming (potential niche) from that whic h it actually consumes (realized niche). Functioning at maximum capacity would typi cally be an unnecessary expenditure of energy, especially when feeding occurs in a niche such as durophagy that is relatively inaccessible to sympatric taxa. Feeding Ecology The cranial architecture and prey capture behavior of H. francisci enable it to exploit hard prey, which is a relatively untapped ecological ni che for aquatic vertebrates. In fishes, durophagy has been associated with high bite forces and low dietary diversity (Wainwright, 1988; Clifton and Motta, 1998). Sp ecies capable of consuming hard prey are morphologically segregated by relative di fferences in bite fo rce and ecologically segregated by the hardness of the prey th ey can consume (Kiltie, 1982; Aguirre et al., 2003). Therefore, durophagy appears to resu lt in niche specialization and competition reduction. This is the case in H. francisci because hard prey (molluscs, echinoderms, benthic crustaceans) comprises approximately 95% of its diet (Strong Jr., 1989; Segura-

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43 Zarzosa et al., 1997). However, Summ ers et al. (2004) suggested that H. francisci goes through on ontogenetic shift to durophagy due to biomechanical changes in its jaw cartilages. It remains to be seen if H. francisci undergoes a reduction in dietary diversity and increased niche specialization over ontoge ny, with associated changes in feeding behavior and performance. A more detailed dietary analys is of neonate and juvenile H. francisci would be needed to determine whether these changes occur. Biomechanical modeling and performan ce testing provide a morphological and behavioral basis from which to interpre t differences in organismal ecology. These analyses determined that H. francisci is capable of generating bite forces an order of magnitude higher than comparably sized S. acanthias (Huber and Motta, 2004), and that H. francisci applies bite force in a way suited for processing hard prey. Differences in the feeding performance of H. francisci and S. acanthias directly coincide with the different feeding niches they occupy (durophagy and piscivory respec tively) (Segura-Zarzosa et al., 1997; Alonso et al., 2002). Therefore, these analyses are of util ity for understanding the diversity of elasmobranch feeding mech anisms at numerous organismal levels (morphology, behavior, ecology), as well as th e selective pressures involved in the evolution of these mechanisms. Heterodontus francisci has the second highest mass-specific bite force of the cartilaginous fishes in which bite force ha s been measured or estimated (Huber and Motta, 2004; Huber et al., 2006, in prep). Relative to body mass, the hardest biting cartilaginous fish studied thus far is H. colliei, which is also durophagous (Johnson, 1967; Ebert, 2003). Neither H. francisci nor H. colliei were comparable in biting ability to the durophagous teleost fishes C. schoepfi L. maximus and the sheepshead Archosargus

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44 probatocephalus. The mass specific bite forces of these teleost fishes, which possess a battery of anatomical specializations asso ciated with durophagy respectively (Hernandez and Motta, 1997; Clifton and Motta, 1998; Korff a nd Wainwright, 2004), were considerably higher than those of the durophagous cartilaginous fishes (Appendix I). Comparative materials testing of the hard pr ey items in the diets of these cartilaginous and teleost fishes would be required to determine the ecological relevance of these differences in bite force. Nonetheless, the bite forces of these fishes collectively indicate that high biting performance, in addition to an atomical specialization, are associated with the consumption of hard prey. Conclusions The heterodontiform sharks, as represented by the horn shark H. francisci, possess a unique combination of morphologi cal and behavioral characteri stics that enab le them to consume hard prey. Although H. francisci bites harder than the average vertebrate of comparable size, on a mass specific basis it is not the most powerful biter in the animal kingdom (Fig. 8). Reptiles, mammals, other fish es, and even some birds are capable of performing as well as or better than H. francisci when body mass is accounted for. This data suggests that factors other than bite for ce magnitude play a significant role in prey capture and processing ability. For H. francisci these factors are molariform teeth, robust jaws, a high leverage jaw-adducting mechanis m, and long duration, cyclically applied bite forces. The durophagous feeding behavior of H. francisci is reflected in its extensive ethmoidal articulation bracing the anterior portion of the upper jaw against the chondrocranium during prey cap ture and processing. Although in situ bite force

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45 measurements provided valuab le information regarding its feeding behavior and ecology, theoretical estimates and restrained bite fo rce measurements were the most effective means of estimating maximum bite force de pending on the availability of deceased specimens and live individuals. Because only a few investigations of biting performance in cartilaginous fishes have been made (Snodgrass and Gilbert, 1967; Evans and Gilbert, 1971; Huber and Motta, 2004; Huber et al., 2005, 2006, in prep), little is known about the role that bite force plays in the ecological and evolutionary success of sharks. Combining theoretical and performance anal yses provides the basis for an in-depth understanding of the link between morphology, behavior, and ecology in sharks, and the role that biomechanics plays in the form and function of shark feeding mechanisms.

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46 Chapter 2: Prey Capture Biomechanics and Feeding Performance of Juvenile Lemon Sharks Negaprion brevirostris Abstract The bite performance of juvenile lemon sharks Negaprion brevirostris was investigated via three-dimens ional static equilibrium an alyses of the jaw adducting musculature and in situ performance trials. Maximum bite force was determined from theoretical analyses involving protrusion of the upper jaw and ranged from 69-217 N from the anterior to posterior-most tooth in the functional row. Equilibrium analyses were also used to model the load ings occurring throughout th e jaw suspension mechanism. During bites without upper jaw protrusion, the ethmoidal articulation is under negligible tension (1 N) while the hyomandibula is under negligible compression (2 N). Bites involving upper jaw protrusion, in which th e ethmoidal articulation is disengaged, substantially increased comp ression of the hyomandibula (60 N), and suggest that the evolution of upper jaw protrusion in elasm obranchs was associated with increased hyomandibular loading, resulting in increased kinesis at the anterior margin of the jaws. Voluntary biting by N. brevirostris involved low magnitude forces (13 N) applied over a short duration (114 ms). The five-fold discrepa ncy between voluntary and theoretical bite force measurements indicates that the effectiveness with which the teeth of N. brevirostris cut prey plays a large role in its pred atory successes. The mass-specific bite

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47 force of N. brevirostris is intermediate among the cartilagi nous fishes in which bite force has been investigated.

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48 Introduction The emergent functional properties of a biomechanical system are best diagnosed in two ways: 1) detailed mechanical analysis of the components of the system; and 2) measurement of the performance of the system. Through these two approaches, the morphological basis of mechanical perfor mance can be identified and performance constraints on a system can be assessed. The el egance of such a research program is in its applicability to all mechanical systems, man-made or biological (Aerts and DeVree, 1993; Long et al., 2004). In recent time the utility of mechanical analyses has been realized in studies of the ecology and evol ution of vertebrate feeding, and has set a precedent for the continued study of vertebrate feeding mechanisms (Lauder, 1991). The feeding mechanisms of the elasmobranch fishes (sharks, skates, and rays) are highly diverse in their functional properties which is largely due to the coupling and decoupling of skeletal elements and muscle systems throughout evolution (Wilga et al., 2001; Dean and Motta, 2004a). Although the basic components of elasmobranch feeding mechanisms are homologous, they have differentia ted in form and function to garner prey resources ranging from plankton to marine mammals (Sims, 1999; Klimley et al., 2001). The functional and ecological diversity of elasmobranch feeding mechanisms is particularly interesting given the small number of kinetic morphological elements on which they are based (Motta, 2004). Elasmobr anch feeding mechanisms are essentially composed of upper and lower jaws that articul ate indirectly with the chondrocranium via mobile hyomandibular cartilages (Fig. 9). In most taxa the upper and lower jaws are movable independently of each other and th e chondrocranium (but see Dean and Motta (2004a)). An extensive range of prey capture behaviors (ram, suction, biting, filter

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Fig. 9. Left lateral view of the cranium, jaws, and hyoid arch of N. brevirostris, with the skin and muscles removed. Tendons and ligaments are indicated. C, ceratohyal; ECN, ectethmoid condyle; HMD, hyomandibula; LCP, ethmopalatine ligament; LHME, external hyoid-mandibular ligament; LHMM, medial hyoid-mandibular ligament; LHPE, external hyomandibula-palatoquadrate ligament; LHPI, internal hyomandibula-palatoquadrate ligament; LPI, postspiracularis ligament; MC, Meckel's cartilage (lower jaw); MR, medial rostral cartilage; NC, nasal capsule; OP, orbital process of palatoquadrate; OT, otic capsule; PMTS, palatoquadrate-mandibular connective tissue sheath; PR, preorbital process; PT, postbital process; SL, suborbital ledge; SS, suborbital shelf; TCHD, constrictor hyoideus dorsalis tendon (modified with permission from Motta and Wilga (1995)). feeding) mirrors the morphological diversity found among elasmobranch feeding mechanisms (Le Boeuf et al., 1987; Klimley et al., 1996; Motta et al., 1997, 2002; Sims, 1999; Huber et al., 2005). Although recent studies of elasmobranch feeding have incorporated functional interpretations of anatomical structures and behaviors (see Motta and Wilga (2001) and Motta (2004) for review), the mechanical basis of functional diversity has largely been treated qualitatively. Kinematic measurements and anatomical descriptions stop short of determining the actual forces exerted by organisms in the environment, which may 49

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50 ultimately dictate ecological success under comp etition for finite resources. For this reason it is necessary to quantify performance measures such as bite force, which has been shown to affect resource partitioning (Kiltie, 1982; Herrel et al., 2004a), ontogenetic changes in feeding ecology (Hernandez and Motta, 1997), dietary diversity (Wainwright, 1988; Clifton and Motta, 1998; Herrel et al., 2004b), and prey handling efficiency (Verwaijen et al., 2002; Van de r Meij et al., 2004). Measurem ent of these forces provides greater resolution of the means by which morphologically and behaviorally diverse elasmobranchs procure equally diverse prey resources. Considerable advances have been made in the understanding of the morphology, behavior, and ecology of shark feeding due to studies involving the lemon shark Negaprion brevirostris a ram-feeding trophic generali st that routinely uses jaw protrusion while capturing prey (Moss, 1972; Wetherbee et al., 1990; Motta and Wilga, 1995; Motta et al., 1997; Sundstrom et al., 2001 ). These studies have determined the anatomical and physiological basis of cran ial kinesis, described the prey capture methodology of N. brevirostris (ram), and elucidated the manner in which prey selection is related to habitat use. However, the direct link between morphology, feeding performance, and ecology has not been established. Two additional questions that remain unanswered in elasmobranch feeding regard the mechanics of jaw protrusion and the manner in which cranial force generation has influenced the evolution of jaw suspen sion mechanisms. Jaw protrusion has been hypothesized in part to increase prey capture and manipulation efficiency by augmenting the cutting ability of teeth, reducing jaw closure time and distance, and enabling greater precision when grasping prey from the substr ate (Springer, 1961; Tricas and McCosker,

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51 1984; Frazzetta and Prange, 1987; Motta et al., 1997; Wilg a et al., 2001). Protrusion reduces jaw closure distance by 26% in N. brevirostris (Motta et al., 1997). Like most modern elasmobranchs, N. brevirostris possesses a hyostylic jaw suspension in which the jaws articulate with the c hondrocranium posteriorly via hyomandibular cartilages and anteriorly via ligamentous attachment s between the ethmoid region of the chondrocranium and the palatal region of the upper jaw (Gregory, 1904; Wilga, 2002) (Fig. 9). Although this is the typical arra ngement found among elasmobranchs, numerous taxa possess variations of the hyostylic jaw suspension mechanism involving either fewer (euhyostyly) or greater (amphistyly) numbers of articulati ons between these elements (Maisey, 1980; Shirai, 1996; Wilga, 2002). Morphological and behavior al investigations have suggested a link between the evolution of upper jaw protrusion and jaw suspension in elasmobranchs such that the shift to hyosty ly, wherein most of the jaw support is borne by the hyomandibula, resulted in freeing up of the anterior margin of the jaws, facilitating greater protrusion (Schaeffer, 1967; Wilga, 2002; H uber et al., 2005). In order to develop a more comprehens ive understanding of ram feeding and the evolution of jaw suspension in elasmobranchs, the goals of this study were to: 1) measure the biting performance of N. brevirostris during voluntary feeding and restrained biting, and compare these measures to theoretical es timates of bite force from modeling of the cranial musculature; 2) determine the load ing regimes occurring th roughout the jaws and suspensorium, and discuss the implications of these loadings for the hyostylic jaw suspension mechanism of N. brevirostris ; 3) validate previously stated hypotheses regarding the mechanical basis of jaw protrusion; and 4) place the bite performance of N.

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52 brevirostris in an ecological and func tional perspective with respect to other cartilaginous fishes. Materials and Methods Experimental Animals Five juvenile N. brevirostris (59 cm – 69 cm TL) were housed at Mote Marine Laboratory’s Center for Tropical Research on Summerland Key, FL in accordance with the guidelines of the Institutional Animal Care and Use Committees of Mote Marine Laboratory and the University of South Florida (IACUC #1882) Individuals were maintained at 27 C in a 12,000 l circular tank on a diet of thread herring Opisthonema oglinum and squid Loligo spp. One side of the tank held a window for viewing. Four additional juvenile N. brevirostris (60 – 69 cm TL) obtained o ff Miami, FL, were frozen until used for morphological analyses. Cranial Morphology Theoretical force generation was modeled in eight of the cranial muscles involved in the expansion (coracomandibularis, coracohyoideus, coracoarcualis, and coracobranchiales), compression (quadrat omandibularis dorsal (1-4) and ventral divisions, preorbitalis dors al and ventral divisions, and levator palatoquadrati), and retraction (levator hyomandibularis ) of the feeding mechanism of N. brevirostris (Fig. 10). Each muscle was excised, unilaterally wher e applicable. Using the tip of the snout as the origin of a three-dimensi onal coordinate system, the posi tions of the jaw joint and the origins and insertions of each muscle were taken by measuring the distances of these points from the X, Y, and Z planes intersecti ng the tip of the snout. From this point, the

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Fig. 10. (A) Left lateral and (B) ventral views of the cranial musculature of N. brevirostris. BA, branchial arches; CC, coracoarcualis; CH, coracohyoideus; CHD, dorsal hyoid constrictor; CHV, ventral hyoid constrictor; CM, coracomandibularis; EP, epaxialis; FA, fin adductor; GR, gill rays; HN, hyomandibular nerve; HYP, hypaxialis; IMD, intermandibularis; LH, levator hyomandibulae; LHPE, external hyomandibula-palatoquadrate ligament; LHPI, internal hyomandibula-palatoquadrate ligament; LP, levator palatoquadrati; LPN, levator palpebrae nictitantis; MC, Meckels cartilage (lower jaw); MN, mandibular branch of trigeminal nerve; NC, nasal capsule; NI, nictitating membrane; OR, orbit; PD, dorsal preorbitalis; PV, ventral preorbitalis; PQ, alatoquadrate (upper jaw); QD, dorsal quadratomandibularis; QV, ventral quadratomandibularis; VSBC, ventral superficial branchial constrictor. The coracobranchiales is located deep to the coracoarcualis (modified with permission from Motta and Wilga (1995)). 53

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54 X-axis was positive moving caudally, the Y-axis moving dorsally, and the Z-axis moving to the left side of the head. For the purposes of this analysis the jaw joint was considered to be the center of rotation of the dual (lateral and medial (Motta and Wilga, 1995)) quadratomandibular jaw articulation. Each muscle was then bisected through its center of mass perpendicular to the princi pal fiber direction and digital images of the cross-sections were taken (JVC DVL9800 camera). Cross-se ctional areas were measured from these images using Sigma Scan Pro 4.01 (SYSTAT Software, Inc., Point Richmond, CA, USA). Three-dimensional positions were also measured for bite points at 0, 25, 50, 75, and 100% of the length along the functional tooth row from the posterior-most tooth. Out-levers were then determined from the three-dimensional coordinates of these points and those of the jaw joint. In-levers we re determined for each lower jaw adductor (quadratomandibularis dorsal (1-4) and ventral divisions, pr eorbitalis dorsal and ventral divisions) from the positions of the jaw joint and each muscles insertion on the lower jaw. Because the ventral quadratomandibularis br oadly attaches to the lateral face of both the upper and lower jaws, its center of mass a nd average muscle fiber direction relative to the lower jaw were used to approximate its m echanical line of action and insertion point. A resultant in-lever for lower jaw adduction was determined by taking a weighted average of the in-levers based on the force produced by their respective muscles. An inlever for jaw abduction was determined from the three-dimensional coordinates of the jaw joint and the insertion of the coracomandi bularis on the lower jaw. In-lever distances for jaw abduction and adduction (resultant) were divided by out-lever distances to the anterior and posterior-most teeth of the lo wer jaw to determine mechanical advantage

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55 ratios for jaw opening and closing. Anatomical nomenclature is based on Motta and Wilga (1995). Theoretical Biomechanical Analysis Anatomical cross-sectional area (A CS ) measurements of each muscle were multiplied by the specific tension of elasmobranch white muscle (T SP ; 289 kN m -2 (Lou et al., 2002)) to determine the maximum tetanic force (P O ) of each: P O = A CS T SP Force vectors were then created for each mu scle from the three-dimensional coordinates of their origins and inserti ons and their respective maxi mum tetanic forces. The force vectors of muscles excised unilaterally were reflected about the Y-plane to represent the forces generated by the musculature on the other side of the head. Three-dimensional static equilibrium analyses of the feeding mechanism of N. brevirostris during prey capture were performed w ith Mathcad 11.1 software (Mathsoft, Inc., Cambridge, MA, USA). Summation of the three-dimensional moments acting on the lower jaw about the jaw join ts (left and right) determin ed theoretical maximum bite force at points corresponding to 0, 25, 50, 75, and 100% of the distance along the functional tooth row from the posterior-mos t tooth. Jaw joint reaction forces were determined for bites occurring at 0 and 100% of the distance along the functional tooth row. Additionally, the mechanical loadings on the suspensorium of N. brevirostris were determined at the ethmoidal and hyomandibular articulations of the jaws with the chondrocranium and hyomandibula respectively. Two separate equilibrium analyses were performed for N. brevirostris, the first of which involved prey capture without upper jaw protrusion, i.e. the ethmoidal articulation

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56 Fig. 11. Forces involved in the static equili brium calculations of th e lower and upper jaws of N. brevirostris (A) during bites without protru sion and (B) during bites with protrusion. FB, bite reaction force; FE, reaction force at the ethmoidal articulation; FH, reaction force at the hyomandibular articulation; FJR, jaw joint reaction force; FLP, force generated by the levator palatoquadrati; FPD, force generated by th e dorsal preorbitalis; FPV, force generated by the ventral preorbitalis; FQD, force generated by the dorsal quadratomandibularis; FQV, force generated by the ventral quadratomandibularis; angle of incidence of FE relative to the articular surface of the upper jaw at the ethmoidal articulation. Arrow size does not indicate force magnitude and angles of force vectors are approximate. remains intact. For prey capture without protrusion, the moments acting on the upper jaw about the ethmoidal articulation were summed to determine the forces acting at the hyomandibular articulation. This was performe d for bites occurring at 0 and 100% of the distance along the functional to oth row. The forces acting at the ethmoidal articulation were then determined via static equilibrium analysis of the upper jaw (Fig. 11a). Static equilibrium conditions for the forces acting on the lower (FBLJB ) and upper jaws (FBUJB) during prey capture without uppe r jaw protrusion were: FBLJB = FBJRB + FBQD (1,2,3,4)B + FBQVB + FBPDB + FBB B= 0 FBUJB = FBHB + FBJRB + FBQD (1,2,3,4)B + FBQVB + FBPDB + FBEB + FBB B= 0

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57 where FBBB is the bite reaction fo rce from a prey item, FBEB is the force at the ethmoidal articulation, FBHB is the force at the hyo mandibular articulation, FBJRB is the jaw joint reaction force, FBQVB is the force generated by the ventral quadratomandibularis, FBQD (1,2,3,4) Bis the force generated by the divisions of the dorsal quadratomandibularis, and FBPDB is the force generated by the dorsal preorbit alis. This analysis makes the assumption that the ventral preorbitalis and levator palatoquadrati, wh ich are the primary actuators of upper jaw protrusion (Motta et al ., 1997), are not active. Protrusion of the upper jaw during prey capture by N. brevirostris involves the disarticulation of the upper jaw from the chondrocranium, precluding compression at the ethmoidal articulation (Motta and Wilg a, 1995). Loading at the hyomandibular articulation is therefore determined from the static equilibrium of the upper jaw. During protrusion, both the ventral preorbitalis and le vator palatoquadrati are active (Motta et al., 1997). The ventral preorbitalis insert s upon the mid-ventral raphe of the quadratomandibularis, which spans the gap be tween the upper and lower jaws (Fig. 10) (Motta and Wilga, 1995). The force gene rated by the ventral preorbitalis (FBPVB) is therefore included in the equi librium conditions for both the lower and upper jaws. Static equilibrium conditions for the forces acti ng on the lower and upper jaws during prey capture with upper jaw protrusion were (Fig. 11b): FBLJB = FBJRB + FBQD (1,2,4,3)B + FBQVB + FBPDB + FBPVB + FBB B= 0 FBUJB = FBHB + FBJRB + FBQD (1,2,3,4)B + FBQVB + FBLPB + FBPDB + FBPVB + FBB B= 0 In addition to the aforemen tioned force variables, FBLPB is the force generated by the levator palatoquadrati. This static model of bite fo rce did not account for changes in position of the included elements associated with the antero-ventral rotation of the upper jaw away

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58 from the chondrocranium that occurs during protrusion. Upper jaw kinesis will slightly modify the relative three-dimensional or ientation of compone nts in the feeding mechanism, which can affect the estimated ma ximum bite force. In analyses both with and without protrusion the hyomandibula was an alyzed as a two-force member, moveable about its articulations with the upper jaw and chondrocranium (Hibbeler, 2004). The moment acting on the lower jaw during jaw opening via the coracomandibularis muscle was used to determine the theore tical maximum jaw opening force of N. brevirostr is as well. To investigate the mechanical basis of upper jaw protrusion in N. brevirostris and the extent to which variable muscle activity can affect protrusi on, static equilibrium models of the upper and lower jaws were co mpared with and without activity of the ventral preorbitalis, levator palatoquadrati, and coracomandibularis. Contraction of the ventral preorbitalis and levator palatoquadr ati mediates anterior motion of the jaws during protrusion (Moss, 1972; Wilga et al., 200 1). Moss (1972) and Wilga et al. (2001) proposed that contraction of the quadratomandibularis and do rsal preorbitalis while the lower jaw was held in the depressed state vi a activity of the coracomandibularis or from resistance provided by a prey item would cau se the upper jaw to be depressed as well. The quadratomandibularis and dorsal preorbitalis span the upper and lower jaws such that their contractile force will cause the jaws to move towards e ach other in the dorso-ventral plane. Bite Performance Measurements Bite performance measurements were pe rformed with a single point load cell (Amcells Corp., Carlsbad, CA, USA) to which custom designed stainless steel lever arms

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59 were attached. A P-3500 strain indicator (Vishay Measurements Group, Raleigh, NC, USA) provided transducer excitation and si gnal conditioning, and data were acquired via a 6020E data acquisition board and LabVIEW 6.0 software (National Instruments Corp., Austin, TX, USA). Free-swimming N. brevirostris were trained to vol untarily bite the transducer by wrapping it in s quid and presenting it to the sh arks after they were starved for several days. Fifteen measurements duri ng which the transducer was bitten between the tips of the sharks’ jaws were taken from each animal. Placement of the transducer in the mouth was verified via high-speed vide ography (250 fps) of the bite performance trials with a Redlake PCI-1000 digital vide o system (Redlake MASD, San Diego, CA, USA). The modified single-point load cell av erages the signals generated by four strain gages in a full Wheatstone bridge such that the device is insensitive to the position on the lever arms at which force is applied. Therefor e, calibration of the device did not require knowledge of the point at which a shark bit th e lever arms. The following variables were quantified from the trials eliciting the five highest bite forces: maximum force (N), duration of force application (ms), time to maximum force (ms), rising slope of forcetime curve (N sP-1P), duration at maximum force (ms), time from maximum force to end of force production (“time away from maximum force” (ms)), falling slope of force-time curve (N sP-1P), and impulse ( I ), which is the integrated area under the force-time curve (kg m sP-1P) from the initiation of for ce generation to its cessation: I = F dt To determine whether any behavioral artif acts were associated with biting a steel transducer, N. brevirostris were also filmed (250 fps) while eating pieces of O. oglinum cut to the same size as the bite force trans ducer (“fish bites”). A series of kinematic

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60 variables were then quantifie d from these video sequences, as well as those from the in situ bite performance trials (transducer bites). Us ing Redlake Motionscope 2.01 (Redlake, MASD, San Diego, CA, USA) a nd Sigma Scan Pro 4.01 (SYSTAT Software, Inc., Point Richmond, CA, USA) software, th e following variables were measured from both fish and transducer bites: distance, dur ation, velocity, and accel eration of lower jaw depression, lower jaw elevation, upper jaw pr otrusion, and head depression, maximum gape, time to maximum gape, time to onset of lower jaw elevation, tim e to onset of head depression, and cranial elevation angle. All kinematic variables were quantified using discrete cranial landmarks as referenc e points (Motta et al., 1997). Restrained bite performance measur ements were obtained by removing the experimental animals one at a time from the holding tank and restraining them on a table. Once they had opened their jaws an adequate distance the transducer was placed between the tips of their jaws, which elicited an aggressive bite. Three measurements were acquired from each individual in this way. Max imum bite force, time to maximum force, and time away from maximum force were quantified from re strained bites. Statistical Analysis All bite performance and kinematic variables were log 10 -transformed and linearly regressed against body mass to remove the eff ects of size. Studentized residuals were saved from each regression for subseque nt analysis (Quinn and Keough, 2002). The single maximum in situ bite force and its associated performance measurements from each individual were used to create a profile of maximum bite performance for N. brevirostris These individual maximum performance values were also used to compare the maximum bite forces from theoretical, in sit u, and restrained methods of determining

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61 bite force via one-way ANOVA, and to compare the dynamics of the ascending and descending portions of the bite performance wa veforms. Student's t-tests were used to identify differences between times to and aw ay from maximum force within and between in situ and restrained biting trials, as well as to compare the rising and falling slopes of the force-time curves for in situ biting trials. Principal components anal yses (PCA) based on correlation matrices of the studentized residuals from the five highest bite force values and their respective performance measures, as well as the kinematic variables from fish and transducer bites, were used to identify 1) covariation in b ite performance variable s among individuals; 2) covariation in bite performan ce and kinematic variables from in situ bite performance trials; and 3) covariation in kinematic va riables from fish and transducer bites to determine whether biting a steel transdu cer induced behavioral abnormalities. Nonrotated axes explained the grea test amount of variability in each PCA. Variables with factor scores greater than 0.6 were considered to load heavily on their respective principal components (PCs). Kinematic analys es of transducer bi tes generally did not involve head depression, and upper jaw prot rusion was generally obscured by the bite force transducer, resulting in the exclusion of variables associated with these behaviors from the statistical analyses. For analyses 1 and 3, multivariate analysis of variance (MANOVA) was used to compare the factor scores for PCs with eigenvalues greater than 1.0. A one-way MANOVA was performed on the PCs from PCA 1 to determine whether individuals differed in performance m easurements. A two-way, mixed-model MANOVA was performed on the PCs from PCA 3 with individual as the random effect and prey type as the fixed effect to determine whether fish and transducer bites kinematically

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62 differed. The random and fixed effects were tested over the residual and interaction mean squares respectively in this analysis. In addition to PCA 2, stepwise (forward) multiple regressions were used to determine the predictive relationship betw een prey capture kinematics and bite performance variables from in situ biting trials. In these analyses, the kinematic variables were the multiple independent variables and bite performance variables were individually used as the dependent variable. Last ly, mass-specific bite forces from N. brevirostris were compared to the mass-specific bite forc es for the other cartilaginous fishes, the horn shark Heterodontus francisci blacktip shark Carcharhinus limbatus, spiny dogfish Squalus acanthias and white-spotted ratfish Hydrolagus colliei (Huber and Motta, 2004; Huber et al., 2005, 2006, in prep). Sigmas tat 2.03 (SYSTAT Software, Inc., Point Richmond, CA, USA) was used to determine st udentized residuals. All other statistical analyses were performed in SYSTAT 10 (S YSTAT Software, Inc., Point Richmond, CA, USA) with a p-value of 0.05. All si gnificant differences were investigated post-hoc with Tukeys pairwise comparisons test. Results Cranial Biomechanics The quadratomandibularis (dorsal and vent ral divisions), which is the primary jaw adductor, generated more force than any ot her muscle in the feeding mechanism of N. brevirostris (183 N, Fig. 12). The coracobranchiale s generated the most force of the muscles involved in jaw and hyobranchia l abduction (148 N, Fig. 12). The levator hyomandibularis, which is the only muscle i nvolved in the retraction of the feeding

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Fig. 12. Theoretical forces produced by the muscles involved in (A) abduction and (B) adduction of the feeding mechanism of N. brevirostris. CB, coracobranchiales; CC, coracoarcualis; CH, coracohyoideus; CM, coracomandibularis; LP, levator palatoquadrati; PD, dorsal preorbitalis; PV, ventral preorbitalis; QD, dorsal quadratomandibularis; QV, ventral quadratomandibularis. Table 7. Resultant forces occurring during prey capture broken into their principal components in N. brevirostris Variable Resultant (N) F X (N) F Y (N) F Z (N) Resultant Abductive Muscle Force 13 12 -6 0 Resultant Adductive Muscle Force 167 -150 74 0 Resultant Adductive Muscle Force (w/ Prot.) 193 -172 88 0 Opening Force a -5 0 -5 0 Biting Force a 56 0 56 0 Biting Force (w/ Prot.) a 69 0 69 0 Biting Force b 168 0 168 0 Biting Force (w/ Prot.) b 217 0 217 0 negative values indicate forces acting in the negative direction on their respective axes relative to the right side of the head of N. brevirostris a, biting at the tips of the jaws; b, biting at the back of the jaws; Prot., Protrusion 63

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64 mechanism, generated 83 N. During bites in which protrusion does not occur, the principal component of the muscular force adducting the lower jaw was oriented in the X direction (150 N), or anteriorly with respec t to the head (Table 7). The second principal component of the adductive for ce in bites without protrusion was oriented dorsally in the +Y direction (74 N, Table 7). The resolved adductive vector of these forces pulls the lower jaw anterodorsally. The mechanical advantage of the jaw adducting mechanism during bites without protrusion ranged from 0.33 1.06 for anterior and posterior biting, respectively. The theoretical maximum bite force of N. brevirostris ranged from 56-168 N between the anterior and posterior-most teet h in the functional tooth row (Table 7). When lower jaw static equilibrium calculations included activity of the ventral preorbitalis as would be th e case during upper jaw protrusion, the principal components of the resultant muscular force were oriented anteriorly (172 N) and dorsally (88 N) with respect to the head (Table 7). Activity of the ventral preorbitalis had a negligible effect on the mechanical advantage of the jaw adduc ting mechanism, which ranged from 0.34-1.07 for anterior and posterior bi ting when protrusion occurred. The theoretical maximum bite force during bites with protrusion ranged from 69-217 N for anterior and posterior biting, respectively (Table 7). Jaw joint reaction forces were greater for posterior biting (105 N, 89 N) than anterior biting (88 N, 76 N) for bites with and without upper jaw pr otrusion, respectively (Table 8). Anterior biting in both situations placed the jaw joint globally in compression by virtue of local/internal for ces oriented posteroventrally re lative to the articular surface of the joint on the lower jaw, and anterodor sally relative to th at of the upper jaw (Hibbeler, 2004) (Fig. 13). During biting at th e posterior margin of the functional tooth

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65 Fig. 13. Diagrammatic explanation of local ve rsus global forces act ing at articulations within the feeding mechanism of N. brevirostris using the jaw joint as a model. Arrows within the joint represent equilibrium reaction forces relative to the articular surfaces of skeletal elements (local forces). Arrows ac ting on skeletal elements represent forces causing kinesis of those skeletal elements (global forces). row both with and without protrusion, joint r eaction forces were orie nted posterodorsally relative to the articular surface of the lower jaw and anteroventrally relative to that of the upper jaw, placing the jaw joint in tension (Table 8, Fig. 13). Because disarticulation of the upper jaw from the chondrocranium occurs only during protrusion (Motta and Wilga, 1995) it was assumed that compression at the ethmoidal articulation of N. brevirostris would occur only during bites without protrusion. During these bites th e ethmoidal articulation receiv ed a negligible loading of 1 N, oriented anterodorsally relative to th e upper jaw (18 relative to the X-axis). This orientation indicates that th e upper jaw is slightly pulled away from the chondrocranium during bites without protrusion, perhaps placing the ethmopala tine ligament in tension.

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66 Table 8. Mechanical loadings at articul ation points in the f eeding mechanism of N. brevirostris broken into their principal force components Variable Unilat. Force (N) F X (N) F Y (N) F Z (N) Joint Reaction Force a 76 75 -10 0 Joint Reaction Force (w/ Prot.) a 88 87 -10 0 Joint Reaction Force b 89 75 47 0 Joint Reaction Force (w/ Prot.) b 105 87 58 0 Loading at Ethmoidal Artic. a 1 -0.9 0.3 0 Loading at Ethmoidal Artic. (w/ Prot.) a n/a n/a n/a n/a Loading at Ethmoidal Artic. b 1 -0.9 0.3 0 Loading at Ethmoidal Artic. (w/ Prot.) b n/a n/a n/a n/a Loading at Hyomandibular Artic. a 2 0.9 -0.3 -1 Loading at Hyomandibular Artic. (w/ Prot.) a 60 37 -12 -45 Loading at Hyomandibular Artic. b 2 0.9 -0.3 -1 Loading at Hyomandibular Artic. (w/ Prot.) b 60 37 -12 -45 negative values indicate forces acting in the negative direction on their respective axes relative to the right side of the head of N. brevirostris a, biting at the tips of the jaws; b, biting at the back of the jaws; Unilat., Unilateral; Prot., Protrusion Ethmoidal loading did not differ between bites at the anterior and posterior margins of the functional tooth row (Table 8). Loading at the hyomandibular-mandibular articulation was greater during bites with upper jaw protrusion (60 N) than during bites without (2 N) In both situations hyomandibular loading did not differ between anterior and posterior biting. For biting with and without protrusion, the hyomandibul ar-mandibular articulation was loaded posteroventrally and laterally relative to the jaws, while anterodorsally and medially relative to the hyomandibula (T able 8). These local/interna l forces indicate global compression between the distal condyle of the hyomandibula and back of the jaws during

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67 biting both with and without upper jaw prot rusion. Modeling the hyomandibula as a twoforce member assumes either purely compressi ve or purely tensile loading. Deviations from this assumption, as would be likely dur ing dynamic loading, cannot be determined from these analyses. Although a cumulative force of 275 N is ge nerated by the muscles involved in the abduction of the feeding mechanism of N. brevirostris the only muscle actuating depression of the lower jaw is the coracoma ndibularis, which was capable of generating 13 N of force. Accounting for its acute insert ion on the posterior margin of the lower jaw symphysis (26 ) and the mechanical advantage of the jaw abducting mechanism (0.86), the realized jaw opening force at the anterior margin of the functional tooth row was 5 N (Table 7). Mechanics of Jaw Protrusion Static equilibrium calcula tions on the lower jaw of N. brevirostris indicated that the jaw is elevated with greater force in the anterodorsal direction when the ventral preorbitalis is active (194 N) than when it is not (167 N). This finding accounts for the difference between bite forces with and without protrusion. Activity of the coracomandibularis in absence of the vent ral preorbitalis decreased the lower jaw adducting force by 15% (141 N), whereas simulta neous activity of these muscles resulted in a marginal increase in the anterodorsal ly directed adductive force (168 N). The adductive force pulling the upper jaw poster oventrally (167 N) d ecreased by 17% (140 N) during activity of the vent ral preorbitalis, 38% (103 N) during activity of the levator palatoquadrati, and 55% (76 N) during simu ltaneous activity of these two muscles.

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68 The bulk of the adductor musculature of N. brevirostris spans the gap between the upper and lower jaws and act to draw the jaws together. Forces acting externally to this system (coracomandibularis, ventral preorb italis, levator palatoquadrati (Fig. 10)) therefore actuate movement of the jaw system as a whole. Activity of the coracomandibularis added a posteroventrally di rected force of 13 N to the jaw system, while activity of the ventral preorbitalis and leva tor palatoquadrati contributed 27 and 65 N of anterodorsally directed force, respect ively. Simultaneous activation of the ventral preorbitalis and levator palat oquadrati added 92 N of anterodor sally directed force to the jaws, whereas simultaneous activity of all of three muscles generated a net force of 79 N in the anterodorsal direction. When all three muscles were active, 2.5 times more force was generated anteri orly than dorsally. Prey Capture Performance The mean bite force for all individuals during in situ bite performance trials was 13 N, and was applied to the transducer fo r approximately 114 ms (Table 9). It took juvenile N. brevirostris an average of 46 ms to reach maximum bite force at a rate of 470 N s -1 Maximum bite force was sustained for 13 ms and released over the subsequent 55 ms. Times to and away from maximum bite fo rce were statistically equivalent. Maximum bite force was released at 550 N s -1 which was statistically equivalent to the rising slope of the force-time curve. The average impulse generated during biting was 1 kg m s -1 (Table 9). Although the majority of bites analyzed showed single force peaks associated with single bites, double force peaks separated by an averag e of 31 ms were observed in association with a si ngle bite in 12% of the tria ls. Additionally, head-shaking was observed in 46% of the in situ bite performance trials.

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69 Table 9. In situ bite performance data for N. brevirostris Variable Minimum Maximum Mean +/S.E. Maximum Force (N) 6 31 13 +/4 Force Duration (ms) 24 282 114 +/45 Time to Maximum Force (ms) 11 155 46 +/27 Time at Maximum Force (ms) 2 31 13 +/7 Time away from Maximum Force (ms) 3 110 55 +/19 Impulse (kg m s -1 ) 0.1 4 1 +/0.8 Rising Slope of Force-Time Curve (N s -1 ) 172 1083 470 +/166 Falling Slope of Force-Time Curve (N s -1 ) 78 2156 550 +/402 PCA 1 reduced the performance variab les into two PCs (82.4% of variance explained). MANOVA indicat ed no differences in performance measures among individuals using size-corrected data (Wilks Lambda = 0.742, F 8,38 = 0.764, p = 0.636). PC1 revealed substantial covariation in perf ormance measures for all individuals. Every performance variable other than maximum bite force loaded h eavily upon this axis. Maximum bite force was significantly, though weakly, related to impulse only ( p = 0.011, R 2 = 0.251). Impulse had a strong positive relationship with force duration ( p < 0.001, R 2 = 0.862) and negative relationships with the rising ( p = 0.001, R 2 = 0.406) and falling slopes ( p = 0.001, R 2 = 0.402) of the force-time curve. Force duration had significant negative relationshi ps with both the rising (p < 0.001, R 2 = 0.507) and falling ( p < 0.001, R 2 = 0.698) slopes as well (Fig. 14). PCA 2 on kinematic and performance da ta yielded six PCs with eigenvalues greater than 1.0 (89.9% of the variability explained). Seven of the ten variables that loaded heavily on PC 1 were performance variables (all but maximum force). Force duration, time to maximum force, time at maximum force, time away from maximum

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Fig. 14. Linear regressions of log 10 -transformed bite performance variables of N. brevirostris. (A) Force duration (ms) versus impulse (kg m s -1 ). (B) Slope of the force-time curve (N s -1 ) versus impulse (kg m s -1 ). Black circles represent the rising slope; gray triangles represent the falling slope; regression lines fall on top of each other. (C) Slope of the force-time curve (N s -1 ) versus force duration (ms). Black circles represent the rising slope; gray triangles represent the falling slope. 70

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71 Table 10. Principal component lo adings of performance and kinematic variables from bite performance trials of N. brevirostris Variable PC 1 PC 2 PC 3 Lower Jaw Depression Distance 0.137 0.650 0.632 Lower Jaw Depression Duration 0.434 0.716 0.209 Lower Jaw Depression Velocity 0.111 0.347 0.652 Lower Jaw Depression Acceleration 0.251 0.047 0.505 Time to Maximum Gape 0.651 0.590 0.157 Maximum Gape 0.456 0.297 0.009 Onset of Lower Jaw Elevation 0.640 0.402 0.181 Lower Jaw Elevation Distance 0.529 0.448 0.263 Lower Jaw Elevation Duration 0.579 0.283 0.469 Lower Jaw Elevation Velocity 0.138 0.229 0.471 Lower Jaw Elevation Acceleration 0.468 0.092 0.587 Time to Lower Jaw Elevation 0.749 0.469 0.396 Time to Maximum Force 0.882 0.312 0.040 Time at Maximum Force 0.725 0.470 0.071 Time away from Maximum Force 0.614 0.227 0.581 Force Duration 0.824 0.418 0.350 Rising Slope -0.810 0.178 0.030 Falling Slope -0.658 0.392 0.271 Impulse 0.815 0.380 0.277 Maximum Force 0.122 0.128 0.251 Bold values indicate variables considered to load heavily on a given principal component (loading score > 0.600) force, and impulse all loaded positively on PC 1, while the rising and falling slopes of the force-time curve loaded negatively. Time s to maximum gape, onset of lower jaw elevation, and completion of lo wer jaw elevation were the on ly kinematic variables that loaded heavily on PC 1 (Table 10). Maximum force did not load heavily until PC 5 (8.0% of variance explained), and wa s the only variable to do so on this axis. Performance variables did not load heavily upon any ot her axes. A general lack of kinematic

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72 covariation on all principal components is indi cative of highly variable feeding behavior by N. brevirostris (Table 10). Stepwise multiple regression analyses demonstrated more predictive relationships between kinematic and performance variab les than PCA 2. The four performance variables quantifying durations were all predicted by kinematics. Force duration was significantly positively related to the time to ma ximum gape and negatively related to the duration of lower jaw depression (R 2 = 0.382, F 2,22 = 6.812, p = 0.005). Time to maximum force was positively related to the time to onset and negatively related to the acceleration of lower jaw elevation (R 2 = 0.346, F 2,22 = 5.816, p = 0.009). Most notably, time at maximum force was positively related to the acceleration of lower jaw depression, time to maximum gape, and duration of lower ja w elevation, and negatively related to the duration of lower jaw depression and distance of lower jaw elevation (R 2 = 0.581, F 5,19 = 10.72, p < 0.001). Time away from maximum for ce had a weak, but positive relationship to the time to maximum gape (R 2 = 0.191, F 1,23 = 5.445, p = 0.029). Lastly, the rising slope of the force-time curve was positively related to the acceleration of lower jaw elevation and negatively related to the time to maximum gape (R 2 = 0.394, F 2,22 = 7.153, p = 0.004). Neither of the performance variables indicative of the magnitude of loading generated during a bite (maximum force, im pulse) were predicted by regression models of kinematic variables. PCA 3 of kinematic variables from fish and transducer bite s yielded four PCs with eigenvalues greater th an 1.0 (76.4% of variance e xplained). MANOVA indicated no significant differences between prey capture kinematics from the two presentation methods (Wilks Lambda = 1.0, F 4,37 = 0.0, p = 1.0) or between individuals (Wilks

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73 Lambda = 0.710, FB16,113B = 0.841, p = 0.637). Additionally, there were no significant interactions between presentation met hod and individual (Wilk’s Lambda = 0.697, FB16,113B = 0.892, p = 0.580). Methodological Comparison After controlling for the eff ect of body size, theoretical maximum bite force (69 5 N) was significantly greater than in situ (13 4 N) and restrained (19 5 N) bite forces (FB2,10B = 12.699, p = 0.002). In situ and restrained bite forces were equivalent. Times to and away from maximum bite force were equivalent within in situ (46, 55 ms) and restrained (215, 134 ms) bite fo rce measurements. Times to (tB7B = -2.786, p = 0.027) and away (tB7B = -2.646, p = 0.033) from maximum force were significantly longer during restrained bites than during in situ bites. Bite Forces among Cartilaginous Fishes Bite forces among the cartilaginous fishes collectively scaled to body mass with a coefficient of 0.66, approximating the is ometric scaling coefficient of 0.67. Hydrolagus colliei and H. francisci the two durophagous cartilaginous fi shes in this analysis, had the highest mass-specific bite fo rces (1.08, 0.69 respectively). Negaprion brevirostris was intermediate among the cartila ginous fishes (0.01), with C. limbatus and S. acanthias having the lowest mass-specific bite forces (-0.71, -1.39 respectively) (Huber and Motta, 2004; Huber et al., 2005, 2006, in prep).

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74 Discussion Cranial Biomechanics The maximum bite force of juvenile N. brevirostris ranged from 69-217 N along the lower jaw. This range was estimated from bites with protrusion of the upper jaw, and was 23-29% higher than bites not involving pr otrusion. This finding is attributed to the ventral preorbitalis, which plays a dual role in the adduction and pr otrusion of the jaws (Motta et al., 1997). Increased bite force should therefore be added to the list of hypothetical selective pressure s involved in the evoluti on of upper jaw protrusion in elasmobranchs, including increased prey cap ture and manipulation efficiency due to enhanced cutting ability of teeth, more rapi d jaw closure, more precise handling of benthic prey, and the allowance of a hydrodyna mic sub-terminal mouth (Springer, 1961; Moss, 1972; Tricas and McCosker, 1984; Frazzetta and Prange, 1987; Motta et al., 1997; Wilga et al., 2001). Subdivision of the preorb italis muscle in carcharhiniform sharks created a dorsal division serving as a suppl ementary jaw adductor and a ventral division that both adducts the lower jaw and translat es the upper jaw anteroventrally (Wilga et al., 2001). Although protrusion may augment bite force, juvenile N. brevirostris do not bite particularly hard with respect to other cartilaginous fishes, suggesting that factors other than bite force (e.g. tooth cutting mechanics, head-shaking) figure prominently in its prey capture ability. The hypothesized functions of the dorsa l and ventral preorbitalis, levator palatoquadrati, dorsal and ve ntral quadratomandibularis, and coracomandibularis muscles in upper jaw protrusion were supported by th is study (Moss, 1972; Motta et al., 1997; Wilga et al., 2001). During protrusion, the vent ral preorbitalis and levator palatoquadrati

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75 contributed an anteriorly dire cted force of 86 N and a dorsally directed force of 34 N to the jaws. The anteriorly direct ed force is the impetus behi nd anterior motion of the upper jaw. Ventral motion of the upper jaw is accomplished via multiple mechanisms. Staggered firing of the jaw adducting (dorsal and ventral quad ratomandibularis and dorsal preorbitalis) and jaw protruding musc les (levator palatoquadrati and ventral preorbitalis) (Motta et al., 1997) allows the adductors to pul l the upper jaw away from the chondrocranium, after which it is drawn fo rward by the protruding muscles. Ventral movement of the upper jaw frees its ethmoid pr ocess from the orbital notch in the ventral surface of the chondrocranium. Once the upper jaw is clear of the orbital notch, the anteriorly directed force of the jaw prot ruding muscles forces the upper jaw along the anteroventrally sloping palatal fossa of th e chondrocranium. Therefore, both the jaw adducting and protruding muscles contribute to ventral movement of the upper jaw (Motta et al., 1997). Firing of the coracomandibularis during jaw adduction will facilitate ventral movement of the upper as well. This would create a clockwise moment about the jaws relative to the ri ght side of the head such that the upper jaw is pulled down with 18% more force than the lower jaw is pulled up with. Should the coracomandibularis be inactive at this time, as noted by Motta et al (1997), the inertia of a prey item resisting lower jaw elevation could provide the neces sary imbalance to cause this clockwise moment about the jaws. Additional activity fr om the ventral preorbitalis and levator palatoquadrati after the upper jaw has rotated ventrally (Motta et al., 1997) will augment this clockwise moment as well as pull the upper jaw anteriorly.

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76 In contrast to the anteriorly directed adductive force facilitating protrusion in N. brevirostris (Table 7), the principal component of the jaw adducting force of H. francisci is oriented vertically (Huber et al., 2005), illustrating the di sparity in selective pressures between elasmobranchs with different feeding mechanisms. Ram feeding by N. brevirostris involves anterior movement of the upper jaw during protrusion that will assist in capturing elusive prey (Wainwri ght et al., 2001). Convers ely, the processing of hard prey by H. francisci is enhanced by adductive forces generated orthogonal to the occlusal surface of its molariform teeth. Upper jaw protrusion along with rapid elev ation of the lower jaw facilitates rapid closure of the jaws upon prey by decreasing both gape distan ce and the time required to close the jaws (Wilga et al., 2001). Kinematic analyses of transducer and fish bites determined the average velocity of lower jaw elevation by N. brevirostris to be 43.6 cm/s, which is approximately as quick as any elasm obranch for which data is available (FerryGraham, 1998a; Wilga and Motta, 1998a, 2000; Edmonds et al., 2001). Despite the high speed of lower jaw elevation by N. brevirostris, its jaw adducting mechanical advantage (0.34) is higher than those of most ram-f eeding teleosts that feed upon elusive prey (Wainwright and Richard, 1995; Wainwright et al., 2004; Westneat, 2004). By teleost standards, the adductive mechanical advantage of N. brevirostris is better suited for force transmission than velocity transmission. This mechanical advantage is comparable to those of S. acanthias (0.28) and C. limbatus (0.34), which also rely upon rapid jaw kinesis to capture elusive prey (Castro, 1996; Alonso et al., 2002; Huber and Motta, 2004; Huber et al., 2006). However, the adductive mechanical advantage of N. brevirostris is much lower than those of H. francisci (0.51) and H. colliei (0.57), both of

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77 which consume hard prey (Johnson and Hort on, 1972; Segura-Zarzosa et al., 1997; Huber et al., 2005, in prep). Anterior biting placed the jaw joints of N. brevirostris in compression while posterior biting placed the jaw joints in te nsion. Although the ellipsoidal geometry of the lateral jaw articulation will resist compressive joint reaction forces at a variety of gape angles (Motta and Wilga, 1995), tensile joint reaction forces present a larger problem for the mechanical stability of the feeding mechanism (Greaves, 1988, 2000). Tensile joint reaction forces arise when food is bitten between the jaw joint and the resultant jawadducting force vector (mechani cal advantage > 1.0). In such instances the prey item becomes a temporary fulcrum about which the lo wer jaw rotates, placi ng the jaw joints in tension (Greaves, 1988, 2000). In N. brevirostris stabilization of the jaw joints and the jaws articulations with the hyoid arch agai nst tensile loading is accomplished through an extensive set of ligaments. Lateral translat ion between the upper and lower jaws, as would be associated with lateral head-shaking, is resisted via the el lipsoidal concavity of the lateral quadratomandibular articulation a nd the sagittal orientation of the medial quadratomandibular articulation as well (Motta and Wilga, 1995). Lateral head-shaking is commonly used by N. brevirostris to draw its teeth across prey items (Frazzetta and Prange, 1987; Motta et al., 1997). Mechanics and Evolution of Jaw Suspension Analyses of bites without protrusion reveal ed a potential mechanical role of the ethmoidal articulation in elasmobranch feeding mechanisms. During such bites in N. brevirostris the ethmoidal articulation was in negligible tension (1 N) while the hyomandibula was compressed (2 N) between th e posterior margin of the jaws and the

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78 chondrocranium. These respective loadings are the result of a clockwise moment about the upper jaw relative to the right side of the head, and are contingent upon force being generated by the ventral quadratomandibularis from a position posterior to the jaw joint (Figs. 9, 10). The magnitude of hyomandibular loading is low due to the approximately equal moments generated on either side of the ethmoidal articulation by muscle, joint reaction, and bite reaction forces counteracting each other. The minimal tensile loading at the ethmoidal articulation is readily transf erred to compression by moving the origin of the resultant adductive force vector anterior ly along the lower jaw. This modification increases mechanical advantage and or ients the adductive force vector more perpendicularly relative to the lower jaw, causing a counterclockwise moment to be generated about the upper jaw relative to the right side of the head. This counterclockwise moment subsequently pl aces the hyomandibula in tension and the ethmoidal articulation in compression (D.R. Huber, unpub. data). Simultaneous hyomandibular tension and ethmoidal compression are found in H. francisci due to an anatomical arrangement similar to that hypothesized to cause these loadings in N. brevirostris. These findings demonstrate th at the ethmoidal articulation likely acts as a pivot point in the feeding mechanisms of elasmobranchs in which the upper jaw does not disarticulate fr om the chondrocranium during biting (Huber et al., 2005). Maintenance of the ethmoidal artic ulation during biting, high mechanical advantage (0.51), and perpendicularly arranged jaw adducting muscles give H. francisci an ethmoidal loading over 2500% greater than that of N. brevirostris relative to their respective bite forces. The higher mechanical advantage of H. francisci also causes a greater imbalance of moments cranial and caudal to the ethmoidal articulation, resulting

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79 in nearly 800% more hyomandibular loading than N. brevirostris relative to their respective bite forces. Thus, it is probable th at the hyomandibula acts as a tensile element in elasmobranchs in which the ethmoidal articulation is maintained during biting. As such, the structural and materi al properties of hyomandibulae in these taxa may reflect their tensile role. Protrusion of the upper jaw during biting by N. brevirostris creates an antithetical loading regime to that explained above for elasmobranchs in which the ethmoidal articulation remains intact. During protrusi on, disengagement of the upper jaw from the chondrocranium precludes the generation of bending moments on either side of the ethmoidal articulation and cau ses the muscular and reacti on forces acting on the upper jaw to be linearly transmitted to the jaws articulation wi th the hyomandibula. The result of this transmission is a substantial incr ease in compression of the hyomandibula (60 N). During bites involving prot rusion, the hyomandibulae of N. brevirostris are loaded approximately 300% greater relative to bite force than those of H. francisci in which the ethmoidal articulation remains intact (Huber et al. 2005). The posteroventrally and late rally directed compressive force on the jaws at their hyomandibular articulation will create a laterally directed bending moment and torsion about the jaws in the coronal plane. Lateral deflection and ax ial torsion of the posterior region of the jaws is most likely resisted due to the geometric properties afforded by the large mandibular knob and sustentaculum of the lower jaw. The lower jaw is deepest and widest at these structures and therefore best able to resist flexion along the Y and Z-axes in this region due to increased second mo ments of area. The interaction of the second

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80 moments of area along the Y and Z-planes incr eases the polar second moment of area of the jaws, increasing their ability to resist torsion (Hibbeler, 2004). Increased compressive hyomandibular loading associated with upper jaw protrusion may have been relate d to a freeing-up of the anteri or margin of the jaws, and been the mechanical impetus behind evolutionary changes in elasmobranch jaw suspension. Albeit only in two taxa, evidence from N. brevirostris and H. francisci indicate that disengagement of the ethmoidal articulation, which is associated with extensive protrusion of the upper jaw, cause s a shifting from tensile to compressive loading on the hyomandibula, and concentrates th e forces associated with prey capture to the posterior region of the feeding mechan ism. This transition may hypothetically be correlated with the evoluti onary shift from amphistylic to hyostylic jaw suspension mechanisms and increased upper jaw kinesis. The primary supportive structures in an amphistylic jaw suspension are ligamentous attachments between the anterior margin of the upper jaw and chondrocranium. The posterior margins of the upper and lower jaws articulate with the chondrocranium via hyomandibular cartilages that contribute lit tle support and a postorbital articulation between the upper jaw and chondrocranium may or may not be present. Subsequently, the hyomandibulae of early amphistylic sharks were relatively small (Xenacanthida, Palaeospinax ) (Moy-Thomas and Miles, 1971; Wilga, 2002). In hyostyly the hyomandibula is the primary suppor tive element in the feeding mechanism, which is accompanied by reduced ethmoidal or orbital articulations between the upper jaw and chondrocranium. Elasmobranchs po ssessing a suspensory hyomandibula and an orbital articulation are said to posses an orbitostylic variety of the hyostylic jaw

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81 suspension (Gregory, 1904; Maisey, 1980; Wilg a, 2002). The evolution of hyostyly in elasmobranchs was associated with the re duction of the number (l oss of post-orbital articulation) and size of the articulations between the jaws and chondrocranium and shorter, more mobile hyomandibulae orie nted more orthogonal relative to the chondrocranium during biting (Schaeffer, 1967; Moy-Thomas and Miles, 1971; Maisey, 1980, 1985; Cappetta, 1987; Carroll, 1988; Stahl, 1988; Wilga, 2002). These changes are indicative of enhanced jaw kinesis and th e ability to withstand compression by the hyomandibula. Therefore, hyomandibular morphology (as indicativ e of load-bearing ability) may vary concomitantly with pr otrusion ability in elasmobranchs. The morphological diversity of extant elasmobranch feeding mechanisms represents a continuum w ithin the aforementioned jaw suspension mechanisms. Variability in these mechanisms qualitativ ely supports the hypothesized relationships between hyomandibular loading, jaw kine sis, and suspension mechanisms. The hexanchid sharks (sixgill and sevengill) are th e only extant elasmobranchs to retain an amphistylic jaw suspension, including ethmoida l, orbital, and postorbital articulations (Maisey, 1980; Wilga, 2002). Although the post-orbital articulation of the hexanchid sharks can disarticulate duri ng jaw protrusion, the orbital articulation remains intact (Compagno, 1977; Maisey, 1983; Wilga, 2002). Given this morphological arrangement and the suspensorial lo ading results from both N. brevirostris and H. francisci the hyomandibulae of hexanchid sh arks are hypothesized to e xperience low magnitude tensile loading. This is supported by the f act that their hyomandibulae are long, thin, posteriorly directed, and non-suspensory (Wilga, 2002). Presumably a similar loading regime occurs in orbitostylic sharks such as S. acanthias, in which the orbital articulation

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82 remains intact at maximum upper jaw protrusion as well (Wilga, 2002). In contrast, the hyomandibula is the only articulation between the jaws and chondrocranium in batoid feeding mechanisms (euhyostyly (Wilga, 2002)). Based on th e present body of knowledge it would be parsimonious to infer that the batoid hyomandibula is a compressive element. This assertion is st rongly supported by the lesser electric ray Narcine brasiliensis in which medial translation of the hyomandibulae protrudes the jaws. At maximum protrusion the longitudi nal axes of the hyomandibulae line up with those of the jaws, such that the jaws are axia lly buttressed as they are protruded into the sediment in search of benthic prey. Trab ecular reinforcement in both the jaws and hyomandibulae of N. brasiliensis are arranged to resist buckling associated with axial compression (Dean and Motta, 2004a, 2004b; Dean et al., 2005a). Prey Capture Performance Voluntary biting by N. brevirostris involved the rapid application of low magnitude forces (114 ms, 13 N), indicating that maintenance of bite force is not critical to prey capture. The brief duration of low ma gnitude force, equivalence of the times to and away from maximum force, and equivale nce of the rising and falling slopes of the force-time curve demonstrate that biting by N. brevirostris is characterized by quick, snapping bites during which the application of fo rce is no more important than its release. The rapid application of low magnitude forces minimizes the impulse imparted to prey items by N. brevirostris (1 kg m s -1 ). Impulse, which is repr esentative of momentum transfer, is a measure of the effort ex erted upon one body by another (Nauwelaerts and Aerts, 2003). Because momentum is conserved in inelastic collisions, impulse is a proxy for kinetic energy transfer. Low impulse generation by N. brevirostris therefore indicates

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83 that little kinetic energy is needed for su ccessful predation using ram feeding with extensive protrusion to gouge prey. The bite performance profile of N. brevirostris is in stark contrast to that of H. francisci the only other elasmobranch in which voluntary bite performance has been measured. Heterodontus francisci bites harder (95 N) and longer (535 ms) than N. brevirostris which translates into a biting impul se 25 times greater than that of N. brevirostris The dramatic differences in kinetic energy transfer to prey items between N. brevirostris and H. francisci echo the different physical requirements associated with capturing and consuming prey in th eir respective ecological niches. Heterodontus francisci utilizes deliberate, cyclic al, high-magnitude force app lication to crush molluscs, echinoderms, and benthic crustaceans (Strong Jr., 1989; Segura-Zarzosa et al., 1997; Huber et al., 2005). Negaprion brevirostris is a trophic generalist that relies on upper jaw protrusion and a piercing dentition to slas h prey into pieces small enough to consume (Frazzetta and Prange, 1987; Wetherbee et al., 1990; Motta et al., 1997). Although the interplay between dental morphology and the cutting of compliant materials has received neglig ible quantitative attention, limited empirical evidence and physical theory regarding cutting devices has established a fundamental basis from which to interpret the effectiveness with which the teeth of N. brevirostris cut prey (Frazzetta, 1988; Abler, 1992). The teeth of the lower jaw ar e elliptical in cross-section and sharply pointed, making them effective at puncturi ng compliant materials through pressure concentration. Bite force applied along the long itudinal axes of the teeth is concentrated at the minute area of their tips. Having init ially penetrated, friction between a tooths surface and the cutting substrate will shear the substrate, creating stress concentrations

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84 that lead to material ruptur e and further penetration of th e teeth (Frazzetta, 1988; Martin et al., 1998). The teeth of the lower jaw are the first to cont act a prey item (D.R. Huber, pers. obs.) and likely serve to impale the pr ey item until the teeth of the upper jaw can descend. The triangular teeth of the upper jaw in N. brevirostris possess serrations that gradually enlarge from a tooths tip to its base (Frazzetta, 1988). In itial penetration of these teeth will occur through pressure concentr ation. Once a tooth tip has penetrated and its apical edges encounter the prey item, the cutting mechanism changes from pressure concentration to friction-based draw cutti ng (Frazzetta, 1988). As the apical edges of triangular teeth are forced down through the prey item, frictional and reaction forces between the teeth and the prey item will cause shearing and rupture. As the teeth descend further their serrations will come into contact with the compliant substrate. The substrate will bulge between serrations, converting the draw force acting parallel to the apical edge into a reaction force between the bulged materi al and the edges of the serrations, further augmenting rupture of the prey item (Frazze tta, 1988; Motta, 2004). The triangular form of the upper jaws teeth also allows successi ve serrations to continually encounter and sever new substrate, ever wi dening the cut (Abler, 1992). Lateral head shaking augments th e cutting ability of the teeth of N. brevirostris as well. Its effect will primarily be realized at the anterior teeth that are oriented in the transverse plane, in line with the lateral motion of the head. This movement will cause the somewhat laterally oriented cusps of the teeth in the upper jaw to sink into the prey item, as well as direct material into the la teral notches of the teeth (Fig. 11). Stress concentrations within the cutting substrate in crease substantially when they reach this

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85 notch, promoting the rupture of more durab le connective tissues (Motta, 2004). The ability of tiger sharks Galeocerdo cuvier to bite through the shells of large cheloniid sea turtles is primarily attributed to the use of lateral head shakin g and the presence of exaggerated lateral notches on the serrated teeth of its uppe r jaw (Witzell, 1987; Motta, 2004). Notable covariance was identified within and among several bite performance and kinematic variables. Positive relationships between impulse and all force durations, and negative relationships between impulse and th e rising and falling slopes of the force-time curve, indicate that larger kinetic energy tr ansfers to prey items are associated with slower, more deliberate biting. This relationship was also found in H. francisci (Huber et al., 2005). The dependence of kinetic energy transfer on duration was also corroborated by PCA 2, in which the only kinematic vari ables that covaried with performance variables were durations (Tab le 10). The kinematic variab les found to be predictive of biting performance from multiple regression analyses supported the notion that slower, more deliberate behaviors are associated with greater force production as well, with time to maximum gape and the acceleration of lowe r jaw elevation being the most predictive of biting performance. Methodological Comparison The theoretical bite force of juvenile N. brevirostris was substantially greater than the highest in situ bite force measurements obtained, as was found for H. francisci (Huber et al., 2005). While in situ bite force was not indicative of maximum biting ability in either shark, obtaining volunt ary bite force measurements yielded valuable behavioral information in both cases. In contrast to H. francisci restrained bite force measurements

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86 of N. brevirostris were not comparable to theoretical estimates. This discrepancy is again attributed to these animals contrasting pred atory strategies and perhaps to behavioral motivation under restrained condition s. Under restrained circumstances, N. brevirostris shook its head violently from side to side. E ffort was concentrated on using the teeth as cutting devices instead of applying bite force. Conversely, H. francisci did not employ head-shaking, but instead bit th e force transducer vigorously, as it would have bitten and processed a hard prey item co mmon to its durophagous diet (S egura-Zarzosa et al., 1997). Restrained circumstances did apparently motivate more aggressive behavior in N. brevirostris as indicated by the longer times to and away from maximum bite force. Collectively, of the various methods used to determine bite force in N. brevirostris H. francisci, and S. acanthias, theoretical estimates are the most reliable indicator of maximum performance (Huber and Motta, 2004; Huber et al., 2005). Conclusions The jaw adducting musculature of N. brevirostris generates an anteriorly directed force motivating protrusion of the upper jaw, due in part to the action of the ventral preorbitalis. Previous hypotheses regarding th e different roles of the adductive muscles in upper jaw protrusion were corroborated in this study and the ventral preorbitalis was found to increase bite force during protrusion du e to its dual role in adducting the lower jaw and protruding the upper ja w. Mechanical analyses revealed that the hyomandibula of N. brevirostris is a compressive element regardless of whether or not the upper jaw is protruded, and that compression does not occu r at the ethmoidal articulation between the jaws and chondrocranium. This loading regi me may be indicative of a trend in the

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87 evolution of elasmobranch feeding mechan isms, whereby a posterior shifting of the loadings occurring within the jaw suspension and compressive loading on the hyomandibula results in a freeingup of the anterior margin of the jaws, allowing greater jaw kinesis. The benefit of a highly kinetic feeding mechanis m may come at the cost of having a force-inefficient feeding mechanism however, as bite force is fairly low in juvenile N. brevirostris The very low voluntary in situ bite forces generated by juvenile N. brevirostris suggest that the effectiveness with which its teeth cut prey is very important to its predatory success.

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88 Chapter 3: Mechanical consequences of func tional constraint in the feeding mechanism of the whitespotted bamboo shark Chiloscyllium plagiosum Abstract The evolution of elasmobranch jaw suspension mechanisms has involved the decoupling of skeletal elements and has resulte d in enhanced kinesis of the jaws relative to the cranium. The whitespotted bamboo shark Chiloscyllium plagiosum has a hyostylic jaw suspension in which the upper jaw is in capable of dissociating from the cranium during protrusion, and as such is constraine d in its kinetic abil ities. Biomechanical modeling of the feeding mechanism determined that this linkage causes compression between the anterior margin of the jaws and cranium, while placing the hyomandibular cartilages in tension during biting. Theoreti cally releasing this constraint caused a transition to compressive hyo mandibular loading during bi ting. The release of this constraint occurred during th e evolutionary transition from a hyostylic to euhyostylic jaw suspension mechanism in the batoid elasm obranchs (skates and rays), resulting in increased jaw kinesis and presumably the ope ning of new feeding niches. These results suggest that the decoupling of the anterior margin of the jaws from the cranium, which allows increased jaw kinesis, is associated with a transition from tensile to compressive hyomandibular loading. Biomechanical modeling of jaw mechanics in C. plagiosum also predicted a theoretical maximum bite force of 69 N at the anterior tips of the jaws. To validate this, bite forces were measured in live C. plagiosum through voluntary in situ

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89 biting performance trials (29 N), tetanic stimulation of the jaw adducting musculature (53 N), and measurements on restrained indivi duals (51 N). Theoretical, stimulated, and restrained bite force measurements were st atistically equivalent and all greater than measurements from in situ trials, indicating that 1) C. plagiosum can regulate its bite force and 2) restrained and teta nically stimulated bite force measurements are an accurate proxy for maximum bite force in C. plagiosum

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90 Introduction Functional constraints in musculoskeletal systems influence organismal behavior on a number of levels. Variation in muscle geometry and fiber type delimit the temporal dynamics and forces generated during musc ular contraction (Gans and Gaunt, 1991; Curtin et al., 1998; Lou et al., 2002). The mechanical properties of both intraand extramuscular (tendon) connective tissues infl uence the transmission of these forces to skeletal elements (Alexander, 2002; Purs low, 2002). The relative dimensions of articulated segments within the skeleton th en dictate the rate and force with which muscular contractions are transmitted via these elements to the external environment (Westneat, 1994; Carrano, 1999), while the degr ees of freedom between these elements determines the paths of motion along which these transmissions occur. Developmental constraints further limit organismal functi on by canalizing the ontoge netic trajectories allowed in these parameters (Sears, 2004) Ultimately, interactions among these musculoskeletal variables yield a specific ra nge of behaviors that a given organism is capable of performing, often representing trad e-offs between mechan ical stability and skeletal kinesis (Biewener, 1998). The degrees of freedom between adjacent skeletal elements determine the range of motion allowed between those elements and subsequently influence the nature of the mechanical loadings they ar e subject to. Physical constr aints limit freedom of motion, thereby imposing directionally specific loading patterns on skeletal elements. Such patterns are readily observed in the structural (cortical and trabecular) reinforcement patterns of these elements (Currey, 2002; Lieberman et al., 2003; Dean et al., 2005a; Pontzer et al., 2006). Conversely, the decoupling of skeletal elements allows for greater

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91 freedom of motion and consequently more vari able loading regimes as these elements are subjected to diverse internal and exte rnal forces (Herrel et al., 2000). The elasmobranch fishes (sharks, skates, and rays) are capable of remarkable jaw protrusion (> 100% head length (Dean and Motta 2004b)), which is historically due to a series of decouplings between skeletal elem ents and muscular diversification in their feeding mechanisms (Wilga et al., 2001; Wilga, 2002, 2005). Basal elasmobranchs possessed an amphistylic jaw suspension mechanism in which the large otic flange of the upper jaw articulated with the postorbital regi on of the cranium and the palatine process of the upper jaw articulated with the ethmoi dal region of the cranium, supplemented by ligamentous attachments (Fig. 15). The jaws also articulated with the cranium indirectly via a pair of hyomandibular cartilages extending from the medial face of the jaws posterior to the jaw joint to the otic regi on of the cranium. The hyomandibular cartilages are presumed to have contributed little mechanical support to the jaws in these elasmobranchs (Gregory, 1904; Wilga, 2002). Th ese amphistylic sharks are believed to have used ram feeding, over-swimming and gr asping prey between the jaws (Schaeffer, 1967; Carroll, 1988). Amphistyly gave rise to the hyostylic and orbitostylic jaw suspensions of modern elasmobranchs, although the hexanchiform sh arks retain the amphistylic condition with an orbital, not ethmoidal cranio-palatine articulation (Maisey, 1980). In hyostylic and orbitostylic elasmobranchs, the hyomandi bular cartilages are the primary supportive elements between the jaws and cranium. Hyosty ly and orbitostyly diffe r in that the orbital process of the upper jaw articulates with eith er the ethmoidal or orbital region of the cranium respectively (Fig. 15) (Maisey, 1980; Wilga, 2002). The first decoupling event

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Figure 15. Left lateral views of the feeding mechanisms of (A) Cladodont level Cladodus (amphistyly); (B) the sharpnose sevengill shark Heptranchias perlo Hexanchiformes (amphistyly); (C) whitespotted bamboo shark Chiloscyllium plagiosum (hyostyly); (D) lesser electric ray Narcine brasiliensis (euhyostyly). Heptranchias perlo is also representative of the orbitostylic jaw suspension mechanism due to its multiple cranio-palatine articulations. Articulation points are marked with arrows. C, ceratohyal; CR, cranium; E, ethmoidal; H, hyomandibula; L, lower jaw; O, orbital; P, postorbital; U, upper jaw. The feeding mechanism of Cladodus is based upon Schaeffer (1967) and that of N. brasiliensis is based upon Dean and Motta (2004a). involved in the evolution of hyostyly and orbitostyly from amphistyly involved the loss of the postorbital articulation between the upper jaw and cranium due to reductions of the postorbital process and otic flange of the cranium and upper jaw respectively (Maisey, 1980; Wilga, 2002). The second decoupling event involved the evolution of euhyostyly in the batoid elasmobranchs (skates and rays), in which all direct connections between the upper jaw and cranium were lost. The elements of the hyoid arch are dissociated in these fishes, leaving the hyomandibula as the only supportive structure between the jaws and 92

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93 cranium (Fig. 15) (Gregory, 1904; Miyake and McEachran, 1991; Dean and Motta, 2004a). Due to the unresolved phylogenetic position of the batoids, it is unknown whether euhyostyly evolved from hyostyly or orbitostyly (Shirai, 1996; Douady et al., 2003; Winchell et al., 2004). Nonetheless, th e enhanced jaw kinesis afforded by these changes in jaw suspension is believed to ha ve increased the functional versatility of elasmobranch feeding mechanisms, resulting in the ram, suction, biting, and filter feeding mechanisms of modern elasmobranch s (Moss, 1977; Motta, 2004). Although there is mixed sentiment regarding the magnitude of functional consequence associated with these transi tions based upon kinematic data of upper jaw protrusion in a limited number of species (Moss, 1977; Wilga, 2002; Dean and Motta, 2004b), there is no doubt that these decoupling events have resulted in progressively greater kinesis of the jaws relative to the cranium. The diversification of ligamentous attachments and the muscles involved in jaw kine sis have played an integral role in this evolutionary progression towards enhanced jaw kinesis as well (Wilga et al., 2001; Wilga, 2002, 2005). To date, however, only a single study has taken a quantitative approach to studying the biomechanics of elas mobranch jaw suspensions (Huber et al., 2005). The primary objective of the present stud y was to investigate the loading regime occurring throughout the jaws and their articu lations with the cranium in the hyostylic condition, and to speculate regarding the mechan ical consequences of the transition from hyostyly to euhyostyly. The upper jaw of the whitespotted bamboo shark Chiloscyllium plagiosum maintains permanent contact with the ethmoidal region of the cranium during the full range of motion exhibited during feed ing because the orbital process of the upper jaw cannot dissociate from the orbital groove of the cranium. The pa th of motion allowed

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94 Figure 16. Right lateral view of the cranium of C. plagiosum illustrating the constrained linkage between the orbital groove of the cr anium and the orbital process of the upper jaw. The upper jaw is shown in medial view, reflected 180 about its long itudinal axis. The orbital process is a medially directed prominence that extends from the lingual face of the upper jaw into the orbital groove of the cranium. The orbital groove is an anteroventrally sloping concavity extending la terally from the antorbital process of the cranium. During protrusion in C. plagiosum the orbital process of the upper jaw slides along the ventral surface of the orbital gr oove. The anteroventral slope and caudally directed anterior enclosure of the orbita l groove constrain both the trajectory and magnitude of kinesis of the upper jaw, which cannot disarticulate from the orbital groove. CR, cranium; HF, articular facets for the hyom andibular cartilages; OG, orbital groove; OP, orbital process; UJ, upper jaw. during upper jaw protrusion is subsequently conf ined to the antero-ventral slope of the orbital groove (Fig. 16). This condition contra sts that of other hyosty lic sharks in which the upper jaw can be protruded far enough th at the ethmoidal articulation disengages (Motta and Wilga, 1995). Through biomechani cal modeling of the feeding mechanism of C. plagiosum the effects of maintaining and releas ing this constraint on jaw suspension mechanics were determined. Chiloscyllium plagiosum is an obligate suction feeder known to consume a variety to teleost a nd crustacean prey (Compagno, 2001; Lowry,

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95 2005). Therefore, the secondary objective of this study was to compare the biomechanics involved in the expansion, compression, and retr action of the suction feeding mechanism, which is believed to have arisen following the loss of the amphistylic jaw suspension mechanism. Materials and Methods Experimental Animals Four whitespotted bamboo sharks Chiloscyllium plagiosum Bennett (63 – 74 cm TL) were obtained from SeaWorld Adventur e Park in Orlando, FL and housed at the University of South Florida in Tampa, FL in accordance with the guidelines of the Institutional Animal Care and Use Co mmittee (IACUC #1882). Individuals were maintained at 27 C in a 1,500 l semicircular tank on a diet of thread herring Opisthonema oglinum and squid ( Loligo spp.). The planar face of the tank held a window for viewing. Four additional deceased C. plagiosum specimens (55 – 68 cm TL) obtained from SeaWorld Adventure Park in Orlando, FL were frozen until used for morphological analyses. Morphological Analysis Using the tip of the snout as the origin of a three-dimensional coordinate system, the positional coordinates of the origins and insertions of eight muscles involved in the expansion (coracomandibularis, coracohyoideus, coracoarcualis, and coracobranchiales), compression (quadratomandibularis and pr eorbitalis), and retraction (levator palatoquadrati and levator hyomandibular is) of the feeding mechanism of C. plagiosum were measured with a Polhemus Patriot Di gital Tracker (Polhemus, Colchester, VT,

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96 USA) (Fig. 17). Each muscle was then excise d (unilaterally where applicable), bisected through its center of mass perpendicular to the principal fiber direction, and photographed in cross-section with a Nikon C oolpix 4300 digital camer a. Cross-sectional areas were measured from these images using Sigma Scan Pro 4.01 (SYSTAT Software Inc., Point Richmond, CA, USA). Center of mass was estimated by suspending the muscle from a pin and tracing a vertical line down the muscle. After repeating this from another point, the intersection of the two linetracings indicated the center of mass of the muscle. The three-dimensional coordinates of the center of rotation of the quadratomandibular jaw articulation, ethmoidal articulation between the palatal region of the upper jaw and cranium, and the lateral a nd medial articulations of the hyomandibula with the jaws and cranium respectively were de termined with respect to the right side of the head of each individual. Points corresponding to 0 and 100% of the distance along the functional tooth row on the lower jaw from the posterior-most tooth were also determined; 100% is the anterior-most toot h. In-levers and out-levers for lower jaw abduction and adduction were dete rmined from the three-dime nsional coordinates of the muscles and points on the jaws in order to estimate mechanical advantage ratios for the opening and closing of the jaws. The in-lever for jaw abduction was the distance from the center of rotation of the jaw joint to the in sertion of the coracoma ndibularis on the lower jaw. In-levers for each jaw adducting muscle (quadratomandibularis and preorbitalis) were the distances from the center of rotation of the jaw joint to the origin of each muscle on the lower jaw. A weighted average of th e adductive in-levers was determined based on the forces produced by their respective muscle s. The abductive and weighted adductive

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Figure 17. Left lateral (A) and ventral (B) views of the cranial and branchial musculature of C. plagiosum. AMH, adductor mandibulohyoideus; CC, coracoarcualis; CH, coracohyoideus; CHD, dorsal hyoid constrictor; CHV, ventral hyoid constrictor; CM, coracomandibularis; CO, coracoid bar; CR, cranium; CU, cucullaris; EP, epaxialis; HMD, hyomandibular cartilage; IH, interhyoideus; IM, intermandibularis; LH, levator hyomandibularis; LJ, lower jaw; LP, levator palatoquadrati; NC, nasal capsule; PO, preorbitalis; QM, quadratomandibularis; SP, spiracularis; UJ, upper jaw; VSBC, ventral superficial branchial constrictor. The intermandibularis (IMD) and interhyoideus (IH) have been partially removed to reveal the ventral musculature. The coracobranchiales (not shown) are located deep to the coracoarcualis (CC). 97

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98 in-levers were divided by the out-lever dist ance from the center of rotation of the jaw joint to the tip of the anterior-most tooth of the lower jaw to determine mechanical advantage ratios for jaw abduction and adduc tion (Fig 18a). A mechanical advantage ratio for jaw adduction at the posterior margin of the functional tooth row was determined in this way as well. Anatomical nomenclat ure is based on Motta and Wilga (1999) and Goto (2001). Theoretical Force Generation Cross-sectional area (A CS ) measurements of the eight muscles were multiplied by the specific tension (T SP ) of elasmobranch white muscle (289 kN/m 2 (Lou et al., 2002)) to determine the theoretical maximum tetanic force (P O ) of each: P O = A CS T SP Force vectors for each muscle were then constructed from their maximum tetanic forces and the three-dimensional coordinates of their origins and insertions. The force vectors of muscles excised unilaterally were reflected about the Y-plane to represent the forces generated by the musculature on the other side of the head. Mathcad 11.1 software (Mathsoft, Inc., Cambridge, MA, USA) was used to calculate a static equilibrium model of the forces acti ng on the jaws of C. plagiosum during prey capture. The moments generated by the adductive musculature about the jaw joints were us ed to determine the theoretical maximum bite force and resulting jaw joint reaction forces for each individual (F B F JR Fig. 18b). Maximum bite force was modeled at points 0 and 100% of the distance along the functional tooth ro w from the posterior-most tooth. Manipulation of fresh dead specimens revealed that the upper jaw does not disarticulate from the cranium during jaw abduction and adduction (D.R. Huber, pers. obs.). The

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99 upper jaw is functionally constrained to an anteroventrally path of motion due to its articulation with the orbital groove of the cranium and its abutment with the ventral surface of the nasal capsule. The orbital proce ss of the upper jaw is a medially directed prominence extending from the lingual face of the palatal region of the upper jaw. At rest, the orbital process sits within the caudal portion of the orbital groove on the lateral edge of the antorbita l process of the cranium (Motta and Wilga, 1999) (Fig. 16). During manual protrusion of the upper jaw, the orbita l process slides anteriorly and somewhat ventrally along the orbital groove, never losing contact betw een the articular surfaces. This articulation is maintained even at maximum protrusion when the ligamentous attachments between the upper jaw and craniu m are pulled taught because the rostral end of the orbital groove is enclosed by a caudall y directed cup-shaped lateral expansion of the antorbital process. Provided that during biting the upper jaw remains in contact with the ethmoid region of the cranium anteriorly and th e hyomandibula posteriorly, the mechanical loadings at these articular points can be calculated. Loadings at the ethmoidal and hyomandibular articulations were determined for bites occurring at 0% and 100% of the distance along the functional tooth row. Summation of moments from muscular forces acting on the upper jaw about the ethmoidal articulation was us ed to determine the force acting at the hyomandi bular articulation (F H Fig. 18b). The hyomandibula was modeled as a two-force member, moveable about its articulations with both the upper jaw and cranium (Hibbeler, 2004). The force ac ting through the hyomandibula was then determined from its three-dimensional orientation and the force acti ng at its articulation with the jaws. The force acting at the ethmoi dal articulation was subsequently determined

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100 Figure 18. Schematic diagram of the jaws of C. plagiosum indicating (A) variables for lever ratio analysis and (B) th e forces involved in static eq uilibrium calculations of the upper and lower jaws. AB, resolved in-lev er for jaw adduction; AC, out-lever; BD, resolved adductive muscle force vector; PBOB, maximum tetanic tension; FBBB, bite reaction force; FBEB, reaction force at the et hmoidal articulation; FBHB, reaction force at the hyomandibular articulation; FBJRB, jaw joint reaction force; FBPOB, force generated by the preorbitalis FBQMB, force generated by the quadratom andibularis; Arrow size does not indicate force magnitude and angles of force vectors are approximate.

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101 from static equilibrium calculations of the upper jaw (FBEB, Fig. 18b). Static equilibrium conditions for forces acting on the lower (FBLJB ) and upper jaws (FBUJB) were: FBLJB = FBJRB + FBQMB + FBPOB + FBB B= 0 FBUJB = FBJRB + FBHB + FBQMB + FBEB + FBB B= 0 where FBBB is the bite reaction fo rce from a prey item, FBEB is the force at the ethmoidal articulation, FBHB is the force at the hyo mandibular articulation, FBJRB is the jaw joint reaction force, FBPOB is the force generated by the preorbitalis, and FBQMB is the force generated by the quadratomandibularis. The moment acting on the lower jaw during jaw opening via the coracomandibularis muscle was used to de termine the theoretical maximum jaw opening force of C. plagiosum as well. If the upper jaw was permitted the freedom of motion to disarticulate from the cranium during prot rusion, as is found in the lemon shark Negaprion brevirostris (Motta and Wilga, 1995), the hyomandibula would be the only element in the jaw suspension mechanism of C. plagiosum to receive loading during biting. To identify the loadi ng on the hyomandibula during th is hypothetical situation a second static equilibrium model of the upper jaw was developed, which lacked an ethmoidal force: FBUJB = FBJRB + FBHB + FBQMB + FBB B= 0 Bite Force Measurement For comparison with theoretical estimates of maximum bite force in C. plagiosum bite force measurements were ac quired from four individuals through voluntary in situ bite force trials, measurements while the animals were physically restrained, and through tetanic stimulation of the jaw adduc ting musculature. Previous studies have found the restrained and stimulated methods of measuring bite force to be

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102 accurate indicators of maximum bite force (Huber and Motta, 2004; Huber et al., 2005). All bite force measurements were made us ing a single point load cell (Amcells Corp., Carlsbad, CA, USA) with stainle ss steel lever arms. Free-swimming C. plagiosum were trained to voluntarily bite the transducer by wrapping the device in squid and presenting it to them after several days of food de privation. A P-3500 strain indicator (Vishay Measurements Group, Raleigh, NC, USA) was us ed for transducer excitation and signal conditioning. Data were acqui red with a 6020E data acquisition board and LabVIEW 6.0 software (National Instruments Corp., Aus tin, TX, USA). Fifteen measurements during which the transducer was bitten between th e tips of the jaws were taken from each animal, and the single largest bite force from each shark was used for statistical comparisons. In situ bite force measurements were filmed with a Redlake PCI-1000 digital video system (Redlake MASD, San Diego, CA, USA) at 250 frames per second to verify that bites on the transducer occurred between the tips of the jaws. The position at which a shark bit the lever arms did not need to be determined for calibration of the transducer because the single point load cell used in this study aver ages the signals generated by four strain gages in a full Wheatstone bridge su ch that the transducer is insensitive to the position of force application. To identify any be havioral artifacts associated with biting the device, C. plagiosum were also filmed while consuming pieces of O. oglinum cut to the same size as the biting surface of the for ce transducer (hereafter referred to as fish bites). The following kinematic variables were then quantified from transducer and fish bites using Motionscope 2.01 (Redlake MASD San Diego, CA, USA) and Sigma Scan Pro 4.01 software: distance, duration, velocit y, and acceleration of lower jaw depression,

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103 lower jaw elevation, and head depression; times to onset and completion of hyoid depression; maximum gape; time to maximum ga pe; time to onset of lower jaw elevation; time to onset of head depression; cranial elevation angle. Restrained bite force measurements were made by individually removing each C. plagiosum from the experimental tank and rest raining it on a table. Once the animals opened their jaws an adequate distance, the transducer was placed between the anterior teeth, which elicited an aggre ssive bite. Following a recove ry period of approximately 10-15 minutes, the shark was again removed fr om the tank and anaesthetized with MS222 (0.133 g/l). The quadratomandibularis and pr eorbitalis muscles were implanted with stainless steel 22 gauge hypodermic needles connected to a SD9 stimulator (Grass Telefactor, West Warwick, RI, USA) a nd tetanic fusion of these muscles was accomplished via stimulation (10V, 100 Hz, 0.02 ms delay, 3ms pulse width) while the bite force transducer was placed between the anterior tips of the jaws. Three measurements were taken from each individual in both of these experimental protocols. Individuals were ventilated with aerate d seawater for 2 3 minutes between measurements during muscle stimulation experiments. Statistical Analysis Bite force and kinematic variables were log 10 transformed and linearly regressed against body mass to remove th e effects of size. Studentized residuals were saved from each regression for subsequent analysis (Quinn and Keough, 2002). Principal components analyses (PCA) based on a correlation matrix was then used to id entify covari ation in kinematic variables from fish and transducer bites and reduce these variables to a series of non-correlated principal components (PCs), which were subsequently analyzed

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104 to determine whether there were any behavioral artifacts associated with biting the steel transducer. Due to an unbalanced kinematic sampling, one PCA was performed on all kinematic variables describing lower jaw a nd hyoid movements, and a second PCA was performed on kinematic variables describing head depression. To determine whether fish and transducer bite kinematics differed, two-way, mixed-model multivariate analysis of variance (MANOVA) was used to compare the factor scores of PCs with eigenvalues greater than 1.0. In these analyses individual was used as the random effect and prey type as the fixed effect, which was tested over the interaction mean square. Oneway ANOVA on studentized residuals was used to identify significant differences among the theoretical, in situ restrained, and electr ically stimulated methods of determining maximum bite force. Sigmastat 2.03 (SYSTAT Software, Inc., Point Richmond, CA, USA) was used to determine studentized resi duals. All other statis tical analyses were performed in SYSTAT 10 (SYSTAT Software Inc., Point Richmond, CA, USA) with a p-value of 0.05. All significant differences were investigated post-hoc with Tukeys pairwise comparisons test. Results Biomechanical Modeling The quadratomandibularis, which is the primary adductor of the lower jaw, generated the largest force (134 N) of the eight cranial muscles involved in moving the jaws and hyobranchial apparatus during feeding (Table 11). Of the muscles involved in jaw and hyobranchial abduction, the coracoarcu alis and coracohyoideus generated the largest forces (97 N, 58 N respectively). Th e coracomandibularis (m andibular abductor)

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105 generated the least force (23 N) of the abductor musculature. Comparatively, these forces indicate that abduction of the hyoid arch by the coracoarcualis and coracohyoideus may be of greater importance to buccopharyngeal expansion and suc tion generation than mandibular abduction. Relatively small forces were generated by the muscles involved in returning the jaws and hyoid arch to their re sting positions at the end of a bite (levator palatoquadrati (23 N), levato r hyomandibularis (36 N)). Due to its acute insertion angle on the lower jaw (38 ), only 61% of the force generated by the coracomandibul aris initiated abduction of the lower jaw (14 N). After accounting for the mechanical advantage of the jaw abducting mechanism (0.84), the lower jaw was depressed with a force of 12 N (Table 12). The coracohyoideus (58 N) inserted onto the hyoid arch at 56 resulting in a force of 48 N initiating hyoid arch abduction. The mechanical advantage over hyoid arch abduction is approximately 1.0 because the coracohyoideus inserts onto the distal tips of the ceratohyal cartilages, the lower lever arms of the hyoid arch. Nearly four times more force is dedicated to initiating hyoid arch abduction than lower jaw abduction, corroborating the role of the hyoid arch in suction generation. The resultant adductive force generate d about the lower jaw (169 N) had its principal component oriented vertically al ong the Y-axis (140 N), with the secondary component oriented anteriorly on the X-axis (94 N). This orientation indicates that the adductive muscular force primarily elevates the lower jaw, but also forces the jaw apparatus anteriorly, facilitating jaw pr otrusion during adduction. The mechanical advantage of the jaw-adducting mechanism range d from 0.43 at the an terior tip of the lower jaw to 0.83 at the posterior margin of the functional tooth row. The combination of

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106 Table 11. Theoretical maximum forces gene rated by the cranial musculature during the gape cycle in C. plagiosum Action Muscle Theoretical Max. Force (N) Jaw/Hyobranchial Expansion Coracomandibularis 23 Coracohyoideus 58 Coracoarcualis 97* Coracobranchiales 36* Jaw Adduction Quadratomandibularis 134 Preorbitalis 56* Jaw/Hyobranchial Retraction Levator palatoquadrati 23* Levator hyomandibularis 36* Values are means S.E.M. *Bilateral muscle force for paired muscles Table 12. Resultant forces occurring during prey capture in C. plagiosum broken into their principal components Variable Resultant (N) F X (N) F Y (N) F Z (N) Resultant Abductive Muscle Force 23 18 -14* 0 Resultant Adductive Muscle Force 169 -94* 140 0 Opening Force a 12 0 -12* 0 Biting Force a 69 0 -69* 0 Biting Force b 127 0 -127* 0 negative values indicate fo rces acting in the negative direction on their respective axes a, biting at the tips of the jaws; b, biting at the back of the jaws

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107 a vertically oriented adductive muscular fo rce and relatively high mechanical advantage yielded a theoretical maximum bite force ra nging from 69 to 127 N between the anterior and posterior bite poi nts (Table 12). Static equilibrium calculations determined that the jaw joints of C. plagiosum are in compression during both anterior (59 N) and posterior (47 N) biting by virtue of posteroventrally and anterodorsally directed forc es relative to the articular surfaces of the lower and upper jaws respectively (Table 13, see Fig. 19 for descrip tion of local versus global forces). Due to large X-axis components, the joint reaction forces for anterior and Table 13. Mechanical loadings at articula tion points in the feeding mechanism of C. plagiosum broken into their principal force components Variable Unilateral Force (N) F X (N) F Y (N) F Z (N) Joint Reaction Force a 59 c 47 -35* 0 Joint Reaction Force b 47 c 47 -6* 0 Ethmoidal Artic. Loading (constrained) a 49 c 18 -46* 0 Ethmoidal Artic. Loading (constrained) b 49 c 18 -46* 0 Ethmoidal Artic. Loading (released) a 0 0 0 0 Ethmoidal Artic. Loading (released) b 0 0 0 0 Hyomandibular Artic. Loading (constrained) a 29 t 12 15 21 Hyomandibular Artic. Loading (constrained) b 29 t 12 15 21 Hyomandibular Artic. Loading (released) a 26 c -12* -15* -18* Hyomandibular Artic. Loading (released) b 26 c -12* -15* -18* negative values indicate forces acting in the negative direction on their respective axes relative to the right side of the head of C. plagiosum a, biting at the tips of the jaws; b, biting at the back of the jaws; c, compressive loading; t, tensile loading

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108 Fig. 19. Diagrammatic explanation of local ve rsus global forces act ing at articulations within the feeding mechanism of C. plagiosum using the jaw joint as a model. Arrows within the joint represent equilibrium reaction forces relative to the articular surfaces of skeletal elements (local forces). Arrows ac ting on skeletal elements represent forces causing kinesis of those skeletal elements (global forces). posterior biting were oriented 37 and 10 above the horizontal plan e relative to the lower jaw, respectively. The latter of these forces will promote shearing within the jaw joints via posterior translation of th e upper jaw relative to the lower jaw. Any shearing forces in the jaw joints must be resisted by the lig amentous array binding the mandibular and hyoid arches together be cause the lower jaw of C. plagiosum lacks an ascending process posterior to the quadratomandi bular articulation to impede the aforementioned translation of the upper jaw (Fig. 15). Ratios of joint r eaction force to bite force for anterior and posterior biting were 1.7 1 and 0.74 respectively. Loading at the ethmoidal articulation betw een the orbital process of the upper jaw and ethmoidal region of the cranium was orie nted posteroventrally relative to the upper

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109 jaw indicating compressive loading at this articulation as well (49 N). Compression between the upper jaw and cranium at the ethm oidal articulation will necessarily invoke frictional forces between these elements, im peding anteroventral tr anslation of the upper jaw during protrusion. Ratios of ethmoidal loadi ng to bite force for anterior and posterior biting were 1.42 and 0.77. Ethmoidal loading was the same for biting at the anterior and posterior bite points. Loading at the articulation between th e upper jaw and hyomandibula during bites with the ethmoidal articulation intact was orie nted posterodorsally a nd medially relative to the upper jaw, and anteroventrally and la terally relative to the hyomandibula. This orientation indicates that the hyomandibula is in tension during biting and that the hyomandibular cartilages act as restrictive elem ents inhibiting the forward translation of the jaws of C. plagiosum As with ethmoidal loading, hyom andibular loading (29 N) was equivalent for anterior and posterior biting. The ratios of hyomandibular loading to bite force for anterior and posterior biting with th e ethmoidal articulation intact were 0.84 and 0.46 (Table 13). Under the hypothetical situation in which the orbital process of the upper jaw is capable of disa rticulating from the or bital groove of the cr anium during protrusion, similar to N. brevirostris (see Theoretical Force Generation in Materials and Methods), the hyomandibular cartilages would be lo aded in compression by virtue of an anteroventrally and laterally directed force relative to the upper jaw and a posterodorsally and medially directed force relative to the hyomandibular cartilages. For this scenario, hyomandibular loading was equiva lent for anterior and poste rior biting (26 N) and the ratios of hyomandibular force to bite force for anterior and posterior biting were 0.75 and 0.41 respectively (Table 13). Theoretical di ssociation of the upper jaw from its only

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110 direct articulation with the cranium w ould cause a reversal of loading on the hyomandibular cartilages such that they act as compressive elements buttressing the jaws against the cranium. Methodological Comparison Theoretical maximum bite forces (69 11 N) from mechanical modeling of jaw adduction in C. plagiosum were equivalent to bite force measurements obtained from the stimulated (53 2 N) and restrained (51 5 N) methods. However, bi te forces from these three methods were all signifi cantly greater than voluntary in situ bite force measurements (29 1 N) (F 3,14 = 15.353, p < 0.001) (Table 14). PCA on lower jaw depression and elevation kinematic data from fish and transducer bites yielded six axes with eigenvectors greater th an 1.0 (89.9% of variance explained), while PCA on head depression kinematic data from fish and tr ansducer bites yielded three axes with eigenvectors greater than 1.0 (97.4% of variance e xplained). MANOVA on these principal components found no significant differences in kinematics between fish and transducer bites, indicating that biting the fo rce transducer did not induce any behavioral abnormalities in C. plagiosum Table 14. Results of one-way ANOVA on differ ent methods of determining bite force at the tips of the jaws in C. plagiosum Theoretical Stimulated Restrained In situ Mean max. S.E.M. (N) 69 11 a 53 2 a 51 5 a 29 1 b Statistically similar values are represented by the same lower case letters. Values are means of the single largest bite force values from each individual.

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111 Discussion Functional Constraint The hyostylic jaw suspension of modern elasmobranchs provides enhanced jaw kinesis relative to the amphist ylic condition due to the loss of the postorbital articulation between the jaws and cranium (Schaeffer, 1967; Maisey, 1980; Wilga, 2002). This enhanced kinesis is believed to have increa sed the functional versat ility of the feeding mechanism, resulting in the diversification of feeding modes in elasmobranchs (Moss, 1977; Motta, 2004). However, diversity within the hyostylic mechanism has been shown to influence the nature of the loading regime occurri ng throughout these feeding mechanisms. Chiloscyllium plagiosum has a hyostylic jaw suspension that differs from those of carcharhinid sharks like N. brevirostris in that its upper jaw is constantly buttressed against the ethmoidal region of th e cranium, even at maximum protrusion, due to the association of the orbital process and orbital groove on these respective structures (Fig. 16). Conversely, the upper jaw of N. brevirostris lacks a constrained linkage to the cranium and can be protruded far enough th at the ethmoidal articulation disengages (Motta and Wilga, 1995). This functional constraint in C. plagiosum limits the range of motion of the upper jaw and imposes a directiona lly specific loading pattern such that the upper jaw is compressed against the ethm oidal region of the cranium and the hyomandibular cartilages are load ed in tension regardless of the position on the jaws at which biting occurs. Compressive ethmoidal and tensile hyomandibular loading have also been identified in the horn shark Heterodontus francisci (Huber et al., 2005). Unlike C. plagiosum the orbital process on the upper jaw of H. francisci is not confined to lie within the orbital groove of the cranium. However, the upper jaw of H. francisci is

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112 closely associated with the anteroventrally sloping palatal fossa of the cranium and is tightly bound to the cranium by ligamentous attachments such that it can only move within the palatal fossa during protrusion and subsequently remains in constant contact with the cranium during the full range of mo tion exhibited by the jaws (Huber et al., 2005). Chiloscyllium plagiosum and H. francisci both have a disequilibrium of muscular forces acting between the upper and lower jaws. The preorbita lis muscles of both sharks span from the anterior portion of the lower jaw to the cranium posterior to the nasal capsule, but anterior to the ethmoidal articul ation. As such, the force produced by the preorbitalis adducts the lower jaw but has no effect on the upper jaw. The quadratomandibularis, which spans the upper and lower jaws, does not act between the jaws and cranium. Taking all other muscular and reaction forces to be equal, the force produced by the preorbitalis causes a net upward translation of the jaws, compressing them into and pivoting them around the ethmoida l articulation. Due to the fact that the origin of the preorbitalis on the cranium is anterior to the ethm oidal articulation, the resulting moment arm of this muscle causes a counterclockwise rotation of the jaws about the ethmoidal articulation relative to the right side of the head. This causes an anteroventral rotation of the posterior margin of the jaws and pu lls the hyomandibular cartilages in tension (Fig. 20). Based upon this loading regime, the hyomandibular cartilages probably limit anterior and ventra l movement of the jaws during biting, in addition to suspending the jaws from the cran ium at rest. This finding may be a general characteristic of all hyostylic sharks in wh ich the ethmoidal articulation remains intact during biting, and in orbitostylic sharks like the spiny dogfish Squalus acanthias in which

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Fig. 20. Right lateral view of the feeding mechanism of C. plagiosum indicating the balance of forces acting on the jaws (A) while the ethmoidal articulation remains intact due to the functional constraint imposed by the association of the orbital process and orbital groove on the upper jaw and cranium respectively (see Materials and Methods for description), and (B) while the functional constraint imposed by the orbital process and orbital groove is theoretically released, allowing the upper jaw to dissociate from the cranium during protrusion of the upper jaw. Black arrows with C indicate compressive loading, black arrows with T indicate tensile loading, and white arrows with black outlining indicate the direction of motion of the jaws due to the net muscular forces acting on the feeding mechanism. During functionally constrained biting (A) the jaws translate upwards, compressing and pivoting about the ethmoidal articulation. The resultant rotation of the jaws pulls the hyomandibular cartilages in tension. When this constraint is theoretically released (B), allowing the jaws to protrude far enough away from the cranium to disengage the ethmoidal articulation, upward translation of the jaws occurs in a linear manner, compressing the hyomandibular cartilages against the cranium. contact at the orbital articulation is maintained during jaw protrusion as well (Wilga and Motta, 1998a; Wilga, 2002). Additionally, in C. plagiosum the hyomandibular cartilages articulate with the chondrocranium via two robust condyles that lie in ellipsoidal fossae and permit antero-ventral movement (Motta and Wilga, 1995; Goto, 2001). The degrees of freedom afforded by this articulation should allow the distal hyomandibular cartilages to be drawn antero-ventrally during pivoting about the ethmoidal articulation without inducing bending strain in these cartilages. 113

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114 Separation of the jaws from the hyomandibul ar cartilages under tensile loading in C. plagiosum is resisted by a complex set of ligaments attaching the hyoid arch to the jaw cartilages (Motta and Wilga, 1995; Goto, 2001). Despite any force-damping due to elastic energy storage in these ligaments, the hyoma ndibular cartilages are rapidly loaded in tension over the course of approximately 430 ms (D.R. Huber, unpub. data). Although the biochemical constituents of hyaline cartilage afford it substantial compressive strength, it has a high tendency to strain under tensile and shear loads (Carte r and Beaupre, 2001; Summers and Long Jr., 2006). For this reason th e prismatically calcified cortex of the hyomandibular cartilages may play a key role in resisting deformation. This mineralized cortex is the interface between the aforementioned array of ligaments and the hyaline core of the hyomandibular cartilages, and may serve to diminish strain transfer from the ligaments to this core. Theoretically releasing the upper jaw from its functional constraint created an antithetical loading regime to that o ccurring under normal conditions. Under these hypothetical circumstances, dissociation of th e upper jaw from the cranium during biting would place the hyomandibular cartilages in compression, again due to the force produced by the preorbitalis. Net upward tran slation of the jaws in the absence of ethmoidal contact precludes pivoting of the ja ws about this articulation, resulting in an upward, linear displacement of the jaws. Because the hyomandibular cartilages lie between the jaws and cranium, upward linea r displacement of the jaws compresses the hyomandibular cartilages against the skull (Fi g. 20). Although this dissociation is not possible in C. plagiosum due to the articulation of the or bital process with the orbital groove, other sharks such as N. brevirostris are capable of extensiv e jaw protrusion such

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115 that the ethmoidal articulati on disengages (Motta and Wilga, 1995). Therefore, in taxa lacking a constrained linkage between th e upper jaw and cranium the hyomandibular cartilages may act as both tensile and compressive elements depending upon the degree of upper jaw protrusion (i.e. whether or not the ethmoidal articula tion remains intact). The freedom of motion associated with dec oupling skeletal elements like the upper jaws and crania of elasmobranchs may cause highly variable loading regi mes (Herrel et al., 2000), and the conflicting demands of tensile and compressive forces may limit the extent to which skeletal elements can be specialized to handle either. The theorized effects of decoupling the ethmoidal articulation in both C. plagiosum and N. brevirostris (Ch. 2) demonstrate the potenti al role of the hyomandibula as a compressive element. Based upon these findings it would be logical to infer that the hyomandibula acts as a compre ssive element in the euhyostylic batoid elasmobranchs (skates and rays), in which all anterior arti culations between the ja ws and cranium have been lost (Wilga, 2002; Dean and Motta 2004a). This permanent decoupling is responsible for the extreme upper jaw protru sion observed in bato ids (> 100% head length), as well as their capacity to protrude the jaws asy mmetrically (Wilga and Motta, 1998b; Dean and Motta, 2004b). Unlike C. plagiosum and H. francisci upper jaw protrusion in batoids is not inhibited by frictional forces resulting from compression at the anterior cranio-palatine articulation either. Although no studies have modeled jaw suspension mechanics in a euhyostylic elasm obranch, anatomical data from the lesser electric ray Narcine brasiliensis supports the role of th e batoid hyomandibula as a compressive element. Medial translation of the hyomandibular cart ilages protrudes the jaws of N. brasiliensis At maximum protrusion th e longitudinal axes of the

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116 hyomandibular cartilages are aligne d with those of the jaws, such that the jaws are axially buttressed as they are protruded. Trabecu lar reinforcement in both the jaws and hyomandibular cartilages of N. brasiliensis are arranged to resist buc kling associated with axial compression (Dean and Motta, 2004b; Dean et al., 2005a). Based upon these findings, it appears that the evolution of euhyostyly from hyostyly and the resulting increase in jaw kinesis are associated with a transition from tensile to compressive hyomandibular loading. Skeletal decoupling of the upper jaw and cranium may have provided the necessary degrees of freedom for increas ed jaw kinesis throughout elasmobranch evolution. However, modifications to the cran ial musculature and skeleton were required to actuate and support this kinesis. The di versification and reor ganization of cranial muscles in carcharhiniform and lamniform sharks is responsible for the increased jaw kinesis observed in these taxa (Compa gno, 1988; Wilga et al., 2001; Wilga, 2005), although the extent of protrusi on still appears to be limited in part by the length of the ethmopalatine ligament connecting the upper jaw to the cranium (Wilga, 2002). The extreme jaw protrusion observed in batoids is made possible by the lack of inhibitory cranio-palatine ligaments, the derivation of novel cranial muscles re lative to sharks, and the diversification of existing cranial musc les (Miyake et al., 1992; Wilga and Motta, 1998b; Dean and Motta, 2004a). Precise contro l of jaw protrusion ma y be facilitated by hyomandibular compression as well. In the absence of cranio-palatine contact, compression at the cranio-hyomandibular arti culation would confer stability to the feeding mechanism and allow the associat ed musculature to pivot the jaws and hyomandibular cartilages about the cranium. Such an arrangement would provide the

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117 bracing required for asymmetric protrusion and repeated prot rusion within a single gape cycle (Dean and Motta, 2004b; Wilga, 2005). The increased load-bearing role of the hyomandibular cartilages would have necessitated structural changes to these elemen ts to avoid catastrophic strain magnitudes. The hyomandibular cartilages of ancestral am phistylic sharks, which are presumed to have contributed little support to the jaws, were thin, poorly calcified elements lying at acute angles relative to the cranium and were more similar in appearance to the branchial arches from which they were derived than to the hyomandibular cartilages of extant sharks (Gregory, 1904; Zangerl and Williams, 1975; Wilga, 2002). The transition from amphistyly to hyostyly, orbitostyly, and euhyostyly in modern elasmobranchs was associated with the shortening, thickening, increased calcification, and more orthogonal orientation of the hyomandibular cartilages re lative to the cranium, all indicative of a greater capacity to receive and distribute loading (Schaeffer, 1967; Moy-Thomas and Miles, 1971; Zangerl and Williams, 1975; Maisey, 1985; Cappetta, 1987; Stahl, 1988; Wilga, 2002). Prey Capture Although numerous studies have alluded to the relative hypert rophication of the jaw and hyobranchial abducting musculature in suction feeding elasmobranchs, particularly of the coracohyoideus and coracobranchiales muscles (Moss, 1965, 1977; Motta and Wilga, 1999, 2001; Mo tta et al., 2002; Motta, 2004), quantitative data in support of this assertion is lacking. While the quadratomandibularis generated the most force in C. plagiosum the coracoarcualis and coracohyoideus muscles both generated large abductive forces, more so than the coracomandibularis and coracobranchiales. A

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118 similar force distribution was identified in comparably sized H. francisci which uses a combination of suction and crushing to captu re prey (Edmonds et al., 2001; Huber et al., 2005). Despite previous assertions, the primar y difference in force distribution of these suction feeders and comparably sized ram-feeding N. brevirostris lies in the force produced by the coracoarcualis, which was n early 50% greater in the suction feeders (Motta et al., 1997; Hube r et al., 2005; Ch. 2). The larger forces produced by the coracoar cualis muscles of the suction feeders relative to N. brevirostris suggests that differences in th e kinetics of hyoid arch abduction play a key role in the ability of the former to generate iner tial suction. The coracoarcualis inserts onto the caudal fascia of the cor acohyoideus and electromyography studies of N. brevirostris S. acanthias and the nurse shark Ginglymostoma cirratum demonstrate overlap in the activity of these muscles duri ng hyoid arch abduction (Motta et al., 1997; Wilga and Motta, 1998a; Matott et al., 2005) The adjacent position and simultaneous activity of these muscles potentially allows th em to act as a serial ly contractile muscle unit during force transmission, and the larger forces produced by the coracoarcualis of C. plagiosum and H. francisci indicates that the hyoid arches of these suction feeders are abducted more forcefully than that of the ram feeding N. brevirostris The magnitude of suction pressure and flow velocity induced in front of the mouth are functions of the rate and magnitude of buccopharyngeal expans ion (Muller et al., 1982; Sanford and Wainwright, 2002; Svanback et al., 2002; Day et al., 2005), bo th of which are augmented by powerful jaw and hyoid abducting muscle s (Van Wassenbergh et al., 2005). As no differences are apparent in the forces produced by the coracomandibularis of C.

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119 plagiosum H. francisci and N. brevirostris, the kinetics of hyoid arch abduction appear to the primary determinant of suction generation in these sharks. The onset of suction pressure generation is coincident with the onset of hyoid depression in largemouth bass Micropterus salmoides, although peak pressure was most coincident with peak gape in both M. salmoides and bluegill sunfish Lepomis macrochirus (Sanford and Wainwright, 2002; Svanb ack et al., 2002; Day et al., 2005). Motta et al. (in prep) also found a relationship be tween hyoid depression and the onset of suction generation in G. cirratum However, there was a sign ificant phase lag between lower jaw depression and sub-ambient pressu re drop within the buccopharyngeal cavity suggesting that hyoid arch abduction is the primary actuator of suction generation in G. cirratum not the depression of the lower jaw (M otta et al., in prep). Another key difference among suction feeding sharks such as C. plagiosum and ram-feeding sharks such as N. brevirostris that allows the former to gene rate suction pressure is the protraction of the large labial cartilages of the suction feed ers during the expansive phase of the gape cycle (Wilga and Motta, 1998a; Edmonds et al., 2001; Motta et al., 2002; Lowry, 2005). Labial cartilage extension late rally occludes the gape, thereby augmented flow velocity into the mouth; for a given rate of volumetric buccopharyngeal expansion, flow velocity into the mouth is inversely pr oportional to the size of the mouth aperture (Lauder, 1979; Day et al., 2005). Despite the fact that orectolobiform shar ks are generally classified as suction feeders (Moss, 1977; Motta et al., 2002), th e jaw adducting mechanical advantage of C. plagiosum (0.43) is comparable to those of numer ous bony fishes considered to be hard prey specialists (mechanical a dvantage > 0.35 (Westneat, 2004)). Chiloscyllium

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120 plagiosum consumes a variety of exoskeletoni zed crustacean prey (Compagno, 2001), yet these quarry do not rival the hardness of the prey of durophagous teleosts and elasmobranchs (Wainwright et al., 1976; Currey, 1980; Korff a nd Wainwright, 2004). Regardless of the extent to which C. plagiosum uses suction or jaw prehension to capture prey, its force-efficient jaw adducting mechanis m is partially attri buted to the derived anterior placement and vertical orientation of the preorbitalis musc le in orectolobiform and heterodontiform sharks (Compagno, 1977). The jaw adducting mechanical advantage of the durophagous heterodontiform shark H. francisci (0.51) is the highest reported for any elasmobranch (Huber et al., 2005). Like H. francisci C. plagiosum had low ratios of joint and suspensorial loading to bite force. Low ratios of articular reaction forc es to bite force are ch aracteristic of high mechanical advantage lever systems, whic h are inherently more stable than low mechanical advantage systems due to a low potential for force transmission to adjacent skeletal elements (Koolstra et al., 1988; Huber et al., 2005). For example, a high leverage jaw adducting mechanism transmits a relativ ely higher proportion of the available muscular force to the object being bitten, resu lting in a relatively lower proportion of the muscular force being balanced by jaw joint reaction forces. Any departures from the static conditions of this an alysis via asymmetries in musculoskeletal function could result in the displacement at articular points thr oughout the feeding mechanism, which must be resisted by adjacent skeletal elements. Therefore, low ratios of articular reaction forces to bite force represent relatively lower forces that must potentially be resisted by these adjacent elements. This type of skeletal force distribution may be adaptive in elasmobranchs because their jaws are suppor ted by mobile hyomandibular cartilages.

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121 Conversely, the transmission of force to adjacent skeletal elements may be less problematic in gnathostomes with well-braced feeding mechanisms like the holostylic holocephalans and autostylic tetrapods in which the upper jaw is fused to the cranium (Grogan and Lund, 2000; Liem et al., 2001) Fusion of the upper jaw and cranium precludes the displacement of elements in the jaw suspension mechanism during asymmetric musculoskeletal function. Methodological Comparison As has been found in previous studie s (Huber and Motta, 2004; Huber et al., 2005), theoretical estimates of maximum bite force in C. plagiosum were statistically equivalent to bite forces obtained from re strained and tetanically stimulated methods. Any of these methods can be used to accu rately estimate maximum bite performance depending upon the availability of live i ndividuals and morphological specimens. Voluntary in situ bite force measurements were subs tantially lower than those of the previous three methods and are not a good proxy for maximum bite performance. Voluntary bite performance measurements do, however, possess a wealth of information regarding biting behavior and kinetic energy tran sfer from predator to prey (Huber et al., 2005; Ch. 4), and highlight the ab ility of these sharks to voluntarily modulate bite force. Conclusions By limiting the degrees of freedom in m echanical systems, functional constraints influence both the kinematic and kinetic proper ties of skeletal elements. The nature of the ethmoidal articulation in C. plagiosum specifies the trajectory and extent of upper jaw protrusion, and in doing so, generates a predictable loading regime of ethmoidal

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122 compression and hyomandibular tension. However, theoretically releasin g this constraint demonstrated that the decoupli ng of skeletal elements result s in more variable loading patterns and that the evoluti onary change from a hyostylic to euhyostylic jaw suspension mechanism in elasmobranchs most likely resulted in a transition to compressive hyomandibular loading and concom itant structural modifications to this element. The feeding mechanism of C. plagiosum exhibits characteristics associated with prey capture via suction and biting. Hypertrophication of the muscles invo lved in abducting the hyoid arch indicates that hyobranchial expansion is a critical factor in the ability of C. plagiosum to generate suction. Its high leverage jaw adducting mechanism, comparable to many durophagous bony and cartilaginous fishes indicates an ability to capture and process hard prey as well. However, its relatively low bite force may exclude C. plagiosum from consuming durophagous prey. Additio nally, the theoretical model of bite force in C. plagiosum was validated by both tetanically stimulated and restrained measurements of bite force, indicating that these methods are accurate in estimating maximum bite force in lieu of conducti ng complex biomechanical analyses.

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123 Chapter 4: Prey Capture Behavior and Perf ormance of Sharks Utilizing Ram, Suction, and Suction-Biting Feeding Methodologies Abstract Different prey capture behaviors often result in functional and behavioral tradeoffs that may constrain feeding performance. Ram, suction, and suction-biting feeding in lemon Negaprion brevirostris whitespotted bamboo Chiloscyllium plagiosum and horn sharks Heterodontus francisci were investigated using high-speed digital videography and in situ bite performance measurements to iden tify attributes unique to each mode of prey capture and constraints that govern shark feeding. Ram feeding by N. brevirostris was characterized by relatively slow jaw m ovements that were highly variable during both the expansive and compressive phases of the gape cycle, accompanied by low bite forces. Suction feeding by C. plagiosum involved extremely rapid jaw movements with low variability during all feed ing behaviors. Kinematic events were among the fastest recorded for any elasmobranch to date and the mass-specific bite force of C. plagiosum was the highest among the three species. Prey capture in H. francisci involves suction to initially capture hard prey, followed by crushing. Expansive phase variables in H. francisci were similar to, although slower than, those of C. plagiosum The compressive phase of H. francisci was relatively fast given its 1) n eed for high bite forces to crush hard prey, and 2) the trade-off between force and velocity in mechanical lever systems. Nonetheless, H. francisci had the highest absolute bite fo rce. Ram, suction, and suction-

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124 biting represent three f unctionally disparate feeding behavi ors in sharks characterized by trade-offs in the quickness and forcefulness of cranial movements, as well as gross morphological differences. Comp arative analyses of these feeding behaviors provide a window into the selective regi mes involved in the evolution and diversification of shark feeding mechanisms.

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125 Introduction Resource acquisition is largely determined by behavior acting w ithin the confines of morphological and functional constraints. These behaviors are under selective pressure to increase the efficiency with which anatomi cal structures are used in the environment, and in some cases apparently supersede such constraints (L iem, 1978; Norton, 1991; Nemeth, 1997a). Feeding specialization can occur along a variety of evolutionary trajectories resulting in behavioral polarization among related taxa (Lauder, 1983; Norton and Brainerd, 1993; Ferry-Graham et al ., 2002a; Wainwright et al., 2004). The polarization of feeding behavior s in the aquatic environment has led to three predominant prey capture methodolog ies: ram, suction, and biting. Ra m feeding involves the predator over-taking its prey and either seizing the prey between its ja ws or engulfing the prey in the oropharyngeal cavity. Prey may be overtaken either by movements of the entire body or jaws alone (Motta, 1984; Wainwright et al., 2001). Suction feeding involves the inertial transport of water and prey into the mouth, and occurs due to a subambient pressure generated within the oropharyngeal cavity caused by the rapid expansion of the mouth and hyobranchial apparatus. In biting, prey are seized by the oral jaws while the predator and prey are essentially stationa ry (Liem, 1980; Wainwright, 1999). Ram and suction are generally associated with the capture of elusive pr ey, whereas biting is generally used to capture substrate-affixed and/ or large, hard prey requiring considerable reduction prior to deglutition (Turingan and Wainwright, 1993; Wainwright, 1999; Alfaro et al., 2001). Implicit in the term behavioral polarization is the notion that these feeding methodologies exist in adaptive isolation, when in fact most taxa use a combination of them (Liem, 1980; Norton, 1991).

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126 The contrasting behavioral requirements associated with capturing prey by ram, suction, and biting can initially be unders tood by examining the relative importance of the different phases of the gape cycle. A typical prey capture attempt involves an expansive phase in which the jaws and hyobranchial apparatus are abducted from their resting positions, followed by a compressive phase in which these elements are retracted, culminating in jaw closure. Lastly, a recovery phase occurs in which these elements are returned to their resting positions. A prepar atory phase may be present initially during which the oropharyngeal cavity is comp ressed (Liem, 1978; Lauder, 1985). The preparatory phase is generally associated w ith inertial suction feeding because initial compression of the feeding mechanism maximizes volumetric expansion of the oropharyngeal cavity, the magnitude of which is a key determinant of suction generation (Van Leeuwen and Muller, 1984; Wainwright et al., 2001; Sanfor d and Wainwright, 2002). Suction feeding is contingent upon a ra pid expansive phase to generate the subambient pressure required to draw water and prey into the mouth. In both ram and biting, the compressive phase takes precedence because predatory success is generally contingent upon the rapid or forceful closure of the jaws on or around the prey item (see Clark and Nelson (1997) and Sims (1999) for exceptions). The different behaviors associated with prey capture using ram, suction, and biting extend beyond the relative importanc e of the gape cycle phases and are intrinsically related to the biomechanics of the feedi ng apparatus. Because force and velocity are inversely proportional in mechanical lever systems (Westneat, 1994), behaviors that require forceful movements, such as the crushing of hard prey, necessitate high mechanical advantage mandibular lever sy stems that maximize the transmission of

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127 force from the cranial musculature to prey items. Conversely, systems in which the velocity of jaw movement is of greater importance have low mechanical advantage mandibular lever systems. For a given musc ular input, the transmission of force and velocity cannot simultaneously be maximized, su ch that an animal lying at one end of this continuum is precluded from enhanced performance at the other end (Westneat, 1994; Wainwright and Shaw, 1999). For example, labrid fishes with low mechanical advantage jaw abducting mechanisms depre ss their lower jaws at higher angular velocities than those with high mechanical a dvantage lever systems (Westneat, 1994). Assessing the relative importanc e of the gape cycle phases in light of the trade-off between force and velocity in lever systems reveals the mechanical basis of performance using ram, suction, and biting. Both the ra te and magnitude of volumetric expansion determine the magnitude of the suction pre ssure and flow velocity generated during suction feeding (Muller et al., 1982; Day et al., 2005). I nvestigations of suction generation and cranial kinematics have demons trated that rapid lo wer jaw depression and hyobranchial expansion, and the close temporal succession of these events respectively are the behavioral keys to effective su ction generation (Laude r, 1980; Nemeth, 1997b; Motta et al., 2002; Sanford a nd Wainwright, 2002; Svanback et al., 2002; Day et al., 2005). Experimental analyses have also dem onstrated that manipulating water movement during suction feeding requires a remarkable synchrony of muscle activity characterized by considerable overlap in activity of an tagonist muscles in the feeding mechanism (Liem, 1978; Lauder, 1980; Alfaro et al., 2001; Matott et al., 2005). Additionally, suction pressure and velocity are augmented by a sma ll, round oral aperture, which minimizes the cross-sectional ar ea through which flow is generated (Lauder, 1979).

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128 Although ram feeding and biting both rely upon the compressive phase for prey capture, they do so in opposed manners. Ra m feeders rely upon ra pid adduction of the lower jaw to secure prey either between the jaws or within the oropharyngeal cavity (Porter and Motta, 2004). Unlik e suction feeders, the compressive phase is generally faster than the expansive phase in ram feed ing sharks (Ferry-Graham, 1998a; Wilga and Motta, 1998a, 2000; Edmonds et al., 2001; Motta et al., 2002). Ram feeders, which are not subject to the same hydrodynamic constraints as suction feeders, generally have large oral apertures allowing them to consume larg er prey and may use lateral head-shaking to reduce large prey prior to deglutition (Motta and Wilga, 2001). Conversely, forceful jaw adduction may be used during biting to either fracture hard prey or dislodge substrateaffixed prey (Hernandez and Motta, 1997; Korff and Wainwright, 2004; Wainwright et al., 2004; Westneat, 2004; Huber et al., 2005). Given the tr ade-off between force and velocity in lever systems, fish utilizing biting should have slower rates of jaw adduction for a given magnitude of adductive force. To determine whether ram, suction, and biting occupy different ends of a biomechanical and functional continuum ba sed on these theoretical and empirical grounds, prey capture kinematics and biting performance were investigated in lemon Negaprion brevirostris whitespotted bamboo Chiloscyllium plagiosum and horn sharks Heterodontus francisci. Negaprion brevirostris is a ram-feeding tr ophic generalist that routinely uses jaw protrusion while capturing prey (Wetherbee et al., 1990; Motta et al., 1997). Chiloscyllium plagiosum is a suction feeder that consumes a variety of bony fishes and crustaceans (Compagno, 2001; Lowry, 2005). Heterodontus francisci is a nocturnal forager of molluscs, echinoderms, and benthic crustaceans that uses suction and biting to

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129 capture prey, which is grasped by the anteri or cuspidate teeth and then crushed by the posterior molariform teeth (Strong Jr., 1989; Segura-Zarzosa et al., 1997; Edmonds et al., 2001; Huber et al., 2005). Materials and Methods Experimental Animals Five horn Heterodontus francisci five lemon Negaprion brevirostris and eight whitespotted bamboo sharks Chiloscyllium plagiosum were maintained in accordance with the guidelines of the Institutional Anim al Care and Use Committee of the University of South Florida (IACUC #1882). Heterodontus francisci (63 cm – 74 cm TL) were housed at the University of S outh Florida (Tampa, FL) at 20 C and N. brevirostris (59 cm – 69 cm TL) at Mote Marine Laboratory ’s Florida Keys Tropical Research Center (Summerland Key, FL) at 28 C. Kinematic analyses of were performed on four C. plagiosum (49 cm – 60 cm TL) at SeaWorld Ente rtainment Park (Orlando, FL), while in situ bite performance trials were performed on four C. plagiosum (63 cm – 74 cm TL) at the University of South Florida, a ll of which were maintained at 27 C. All specimens housed at the University of Sout h Florida were kept in a 1,500 l semicircular tank. Negaprion brevirostris were kept in a 12,000 l circular tank at Mo te Marine Laboratory and C. plagiosum filmed at SeaWorld Entertainment Park were kept in a 600 l rectangular tank. All tanks held windows th rough which videography was performed and all individuals were maintained on thread herring Opisthonema oglinum and squid ( Loligo spp.).

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130 Kinematic Analyses Individuals of all three sp ecies were filmed with a Redlake PCI-1000 digital video system (Redlake MASD, San Diego, CA, US A) at 250 fps. Videography was conducted in the holding tanks for each species by isolating an indi vidual to a region of the tank large enough for them to swim freely. A mi rror was placed in the tank at 45 to the camera to provide simultaneous lateral and ve ntral views. Individuals were filmed while capturing O. oglinum that was cut to either half of their mouth width (0.5W) or their entire mouth width (1W). Fifteen kinematic se quences were recorded for each individual on each type of prey type, which were presented haphazardly. Kinematic variables were quantified using Motionscope 2.01 (Redlake MASD) and Sigma Scan Pro 4.01 (SYSTAT Software Inc., Point Richmond, CA, USA) software. These variables described the expansive and compressive phases of the gape cycle. Variables describing the expansive phase of th e gape cycle were: (1 -4) distance, duration, velocity, and acceleration of lower jaw depre ssion; (5) time from the onset of lower jaw depression until maximum gape; (6) maximum gape distance; (7-8) times to onset of and maximum hyoid depression; a nd (9) cranial elevation angl e. Variables describing the compressive phase were: (10-13) distance, duration, velocity, and acceleration of lower jaw elevation; and (14-15) times to the onset and completion of lower jaw elevation. During the compressive phase, variables describing palatoquadrate protrusion were: (1619) distance, duration, velocity, and accelerat ion of palatoquadrate protrusion; (20-21) times to the onset of and maximum palatoquad rate protrusion; and (22) percent by which palatoquadrate protrusion reduced maximu m gape. Lastly, variables describing head depression during the compressive phase were : (23-26) distance, duration, velocity, and

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131 acceleration of head depression; and (27-28) times to the onset and completion of head depression. In Situ Biting Performance Measurements Bite performance measurements were performed using a single point load cell (SPA series, Amcells Corp., Carlsbad, CA, US A) with stainless steel lever arms, which was calibrated using a digital scale. Fr ee-swimming individuals were trained to voluntarily bite the transducer by wrapping the device in squid ( Loligo spp.) and presenting it to them after several days of starvation. A P-3500 strain indicator (Vishay Measurements Group, Raleigh, NC, USA) was us ed for transducer excitation and signal conditioning. Data were acqui red with a 6020E data acquisition board and LabVIEW 6.0 software (National Instruments Corp., Austi n, TX, USA). Biting performance trials were filmed with a Redlake PCI1000 digital video system at 250 fps to verify that the transducer was bitten between th e tips of their jaws. Fifteen m easurements of bite force in which this was the case were recorded from each animal. The five largest bite force measurements for each were analyzed for ei ght performance variables: maximum force (N), duration of force produc tion (ms), time to maximum force (ms), rising slope of force-time curve (N sP-1P), duration at maximum force (ms), time away from maximum force (ms), falling slope of force-time curve (N sP-1P), and impulse ( I ), which is the integrated area under the force-time curve (kg m sP-1P): I = F dt The impulse of a force is the extent to which that force changes the momentum of another body, in this case the force transducer, and th erefore has the units of momentum (kg m sP1P). The five largest bite forces and their associated performance measures from each

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132 individual were used in a multivariate comparison of biting performance in the three species (see below). The single largest bi te force and its associated performance measurements from each individual were us ed to create a profile of maximum biting performance for each species. The single point load cell used in this study averages the signals generated by four strain gages in a fu ll Wheatstone bridge such that the transducer is insensitive to the position on the lever arms where the bite is a pplied. Therefore, the point at which a shark bit the transducer did not need to be determined from the video sequences. Statistical Analysis All kinematic and bite performance variables were Log 10 transformed and linearly regressed against body mass to remove the e ffects of size. These regressions were performed to avoid the confounding effect s of body size on the scaling of cranial kinematics and force production (Wainwright and Shaw, 1999). Studentized residuals were saved from each regression for subse quent analysis. Both kinematic and bite performance data sets were analyzed in the same manner. To obtain a balanced statistical design for kinematic analysis, the kinematic data had to be divided in to three data subsets comprised of expansive and compressive phase data, palatoquadrate protrusion data, and head depression data. Palatoquadrate pr otrusion data were not collected for C. plagiosum because its large labial cartilages obscure the palatoquadrate in lateral view and movement of the palatoquadrate is not visible in ventral view. Principal components analyses (PCA) based on correlation matrices of studentized residuals were performed to 1) identify covariation among species in each kinematic data set and 2) id entify the effects of prey si ze on prey capture kinematics

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133 within each species. In each PCA, variables with factor scores greater than 0.6 were considered to load heavily on their principal components (P Cs). Analysis of variance with individuals nested within species was used to compare the factor scores for each species on PCs with eigenvalues greater than 1.0. Students ttests were used to compare the rising and falling slopes of the force-time curves and the times to and away from maximum bite force within each species. Coefficients of variation (CV) of each variable for each species were calculated to determ ine whether behavioral polarization in each species is associated with canali zation of prey capture behavior: CV = (Standard Deviation / Mean) 100 From these data, mean coefficients of variation were calculated for the expansive phase, compressive phase, palatoquadrate protrusi on, and head depressi on variable groupings. Model I linear regressions were performed in SigmaStat 2.03 (SYSTAT Software Inc.) in order to obtain studentized re siduals. All other statistical analyses were performed in SYSTAT 10 (SYSTAT Software Inc.) with a p-value of 0.05. All sign ificant differences were investigated post-hoc with Tukeys pairwise comparisons test. Results Kinematic Analysis Negaprion brevirostris captured food using ram feed ing exclusively. Strikes were characterized by an increase in swimming velocity, followed by lower jaw depression and head elevation. The mouth was held agap e for a relatively l ong period of time, and lower jaw elevation, upper jaw protrusion, and h ead depression all began just prior to the food entering the gape. Chiloscyllium plagiosum approached the food apparently using

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134 chemosensory cues. Upon reaching the food, C. plagiosum made an abrupt stop, reoriented its mouth above the food, and rapi dly sucked it into the mouth. The feeding mechanism was expanded and compressed very quickly, with labial cartilage extension occurring during the expansive phase. Head el evation was essentially non-existent. Food was generally captured and transported thr ough the oropharyngeal ca vity in a single suction attempt. Like C. plagiosum H. francisci apparently used chemotaxis to locate food, which was sucked into the mouth via rapid expansion of the feeding mechanism, including labial cart ilage extension. Unlike C. plagiosum food was generally grasped between the teeth and processed with additiona l compressions of the jaws prior to being transported through the oropharyngeal cavity. 0.5W Feeding Trials PCA on expansive and compressive phase kinematic data yielded four axes with eigenvectors greater than 1.0 (73.2% of variance explained). Significant differences were found among species and individuals on the first three PCs. All three species were significantly different on PC1 (F 2,186 = 45.953, p < 0.001) with the factor scores of N. brevirostris greater than those of H. francisci which were greater than those of C. plagiosum (Fig 21). The variables loading heavily on PC1 indicate that the durations and relative onsets on kinematic events during the expansion and compression of the feeding mechanism take the longest amount s of time, occur later, and at the lowest accelerations in N. brevirostris Conversely, these events take the shortest amounts of time, occur relatively earlier, and at the highest accelerations in C. plagiosum (Tables 15, 16). Although there were numerous differe nces among individuals within and among species on PC1 (F 11,186 = 9.344, p < 0.001), no intraspecific differences were found in N. brevirostris

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Figure 21. Principal components analysis of expansive and compressive phase kinematic variables from capture of 0.5W sized food by H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included timings, durations, and accelerations of lower jaw depression, hyoid depression, and lower jaw elevation. Variables loading heavily on PC 2 included the magnitudes of displacement and velocities of lower jaw depression and elevation. When capturing small food items, the lower jaw of H. francisci moved greater distances and at higher velocities of depression and elevation than that of C. plagiosum (PC2), both of which were equivalent to N. brevirostris (F 2,186 = 7.218, p = 0.001) (Table 15, 16; Fig. 21). However, species means indicated that C. plagiosum depressed its lower jaw at a higher velocity than H. francisci. The discrepancy was due to a single H. francisci with extremely rapid lower jaw depression (F 11,186 = 4.272, p < 0.001). Heterodontus francisci and C. plagiosum both had significantly higher factor scores than 135

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136 Table 15. Principal component loadings of kinematic variables from 0.5W feeding trials of H. francisci N. brevirostris and C. plagiosum Expansive & Compressive Variab les PC 1 PC 2 PC 3 PC 4 Lower Jaw Depression Distance 0.136 0.856 0.056 0.271 Lower Jaw Depression Duration 0.830 0.298 0.259 -0.067 Lower Jaw Depression Velocity -0.543 0.669 -0.156 0.345 Lower Jaw Depression Acceleration -0.748 0.314 -0.159 0.259 Time to Maximum Gape 0.902 0.213 0.152 -0.171 Maximum Gape 0.455 0.589 -0.279 0.059 Onset of Hyoid Depression 0.306 0.154 0.661 0.245 Time to Maximum Hyoid Depression 0.798 0.069 0.412 0.108 Onset of Lower Jaw Elevation 0.836 -0.130 0.117 -0.072 Lower Jaw Elevation Distance 0.203 0.788 -0.158 -0.092 Lower Jaw Elevation Duration 0.702 0.021 -0.370 0.428 Lower Jaw Elevation Velocity -0.300 0.617 0.186 -0.453 Lower Jaw Elevation Acceleration -0.600 0.312 0.387 -0.512 Time to Lower Jaw Elevation 0.922 -0.094 -0.081 0.145 Head Angle 0.422 0.054 -0.445 -0.216 Protrusion Variables PC 1 PC 2 PC 3 Onset of Protrusion 0.801 0.460 -0.013 Time to Maximum Protrusion 0.920 0.179 0.142 Protrusion Distance -0.547 0.135 0.713 Protrusion Duration 0.492 -0.631 0.502 Protrusion Velocity -0.770 0.562 0.169 Protrusion Acceleration -0.651 0.588 -0.102 % Gape Reduced -0.233 -0.068 0.747 Head Depression Variables PC 1 PC 2 Onset of Head Depression 0.679 0.465 Time to Maximum Head Depression 0.920 0.128 Head Depression Distance 0.281 -0.938 Head Depression Duration 0.823 -0.526 Head Depression Velocity -0.671 -0.567 Head Depression Acceleration -0.856 0.137 Bold values indicate vari ables considered to load heavily on a given principal component (loading score > 0.600)

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137 Table 16. Kinematic data 0.5W feeding trials of H. francisci N. brevirostris, and C. Plagiosum Expansive & Compressive Variables H. francisci N. brevirostris C. plagiosum Lower Jaw Depression Dist. (cm) 1.4 0.1 1.2 0.1 0.8 0.0 Lower Jaw Depression Dur. (ms) 51.2 2.2 53.1 2.6 26.6 0.9 Lower Jaw Depression Vel. (cm s -1 ) 27.5 1.7 23.5 1.4 30.6 1.3 Lower Jaw Depression Acc. (cm s -2 ) 799.0 84.0 543.1 46.5 1351.5 87.5 Time to Max Gape (ms) 58.6 2.4 61.0 2.8 27.5 0.9 Max Gape (cm) 2.9 0.1 3.2 0.1 1.8 0.0 Onset of Hyoid Depression (ms) 29.2 1.9 23.8 1.6 21.5 0.6 Time to Max Hyoid Depression (ms) 69.5 2.7 69.2 2.8 44.7 1.0 Onset of Lower Jaw Elevation (ms) 76.2 2.7 92.4 4.2 51.8 2.7 Lower Jaw Elevation Dist. (cm) 1.5 0.1 1.2 0.1 0.8 0.0 Lower Jaw Elevation Dur. (ms) 42.9 2.6 48.9 2.1 29.0 1.2 Lower Jaw Elevation Vel. (cm s -1 ) 40.5 2.7 26.7 1.3 29.1 1.8 Lower Jaw Elevation Acc. (cm s -2 ) 1541.0 223.7 615.6 58.0 1318.9 113.2 Time to Lower Jaw Elevation (ms) 119.1 4.2 141.3 4.7 80.7 3.3 Head Angle ( ) 1.8 0.2 7.1 0.6 1.2 0.3 Protrusion Variables H. francisci N. brevirostris C. plagiosum Onset of Protrusion (ms) 87.4 3.4 87.9 5.0 Time to Max Protrusion (ms) 112.1 3.7 121.6 5.9 Protrusion Dist. (cm) 0.8 0.0 0.5 0.0 Protrusion Dur. (ms) 24.7 1.2 33.7 2.5 Protrusion Vel. (cm s -1 ) 37.9 2.4 16.7 1.2 Protrusion Acc. (cm s -2 ) 1557.5 204.2 673.2 82.6 % Gape Reduced 27.7 1.3 15.5 0.9 Head Depression Variables H. francisci N. brevirostris C. plagiosum Onset of Head Depression (ms) 80.6 5.4 86.0 5.2 64.0 3.7 Time to Max Head Depression (ms) 116.4 7.0 119.0 6.6 87.0 6.6 Head Depression Dist. (cm) 0.9 0.1 0.8 0.1 0.7 0.1 Head Depression Dur. (ms) 35.8 3.2 33.0 3.1 23.0 4.4 Head Depression Vel. (cm s -1 ) 27.0 2.0 23.5 1.6 31.0 3.7 Head Depression Acc. (cm s -2 ) 1115.0 251.7 974.4 134.3 1456.5 241.1 *Values are means one standard error Acc., Acceleration; Dist., Distance ; Dur., Duration; Vel., Velocity

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Figure 22. Principal components analysis of palatoquadrate protrusion kinematic variables from capture of 0.5W sized food by H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included timings, velocity, and acceleration of palatoquadrate protrusion. Palatoquadrate protrusion duration was the only variable to load heavily on PC 2. N. brevirostris on PC3 (F 2,186 = 15.512, p < 0.001), on which the only variable to load heavily was time to onset of hyoid depression. However, species means demonstrate that the time to onset of hyoid depression in N. brevirostris (24 ms) was intermediate to those of H. francisci (29 ms) and C. plagiosum (22 ms) (Tables 15, 16). The comparable times to onset of hyoid depression among the three species coupled with the relatively early time to maximum hyoid depression in C. plagiosum (Tables 15, 16) indicates that hyoid depression occurs most rapidly in this suction feeding species. PCA on palatoquadrate protrusion kinematics for small food items yielded three axes with eigenvectors greater than 1.0 (82.4% of variance explained). Significant 138

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139 differences were found among species and in dividuals on all three PCs. Significant differences between N. brevirostris and H. francisci on PC1 (F 1,102 = 14.660, p < 0.001) and PC2 (F 1,102 = 43.950, p < 0.001) indicated that palatoquadrate protrusion occurred over a longer period of time and at a slower rate in N. brevirostris (Tables 15, 16; Fig. 22). Heterodontus francisci had significantly higher factor loadings than N. brevirostris on PC3 (F 1,102 = 11.493, p = 0.001) indicating that its pa latoquadrate is protruded a greater distance and reduces maximum ga pe to a greater extent than in N. brevirostris (Tables 15, 16). Significant intraspe cific variability was found within H. francisci on all three axes (PC1, F 8, 102 = 4.611, p < 0.001; PC2, F 8,102 = 6.000, p < 0.001; PC3, F 8,102 = 3.596, p = 0.001). PCA on head depression kinema tics for small food items yielded two axes with eigenvectors greater than 1.0 ( 82.9% of variance explained). No significant differences were found on either PC (Fig. 23). 1W Feeding Trials PCA on expansive and compressive phase kinematics for large food items yielded five axes with eige nvectors greater than 1.0 (81.1% of variance explained). Significant differences were found among species and individuals on PCs 1, 2, and 5, while significant differences were found among species on PC3. Both H. francisci and N. brevirostris had significantly higher factor scores than C. plagiosum on PC1 (F 2,179 = 26.818, p < 0.001). As was found for small food, variable loadings indicate that in general the durations and relative onsets on kinematic events during the expansion and compression of the feeding mechanism ta ke longer, and occur later and at lower accelerations in N. brevirostris as compared to C. plagiosum (Tables 17, 18). Unlike small food, however, the cap ture of large food by H. francisci was equivalent to that of N.

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Figure 23. Principal components analysis of head depression kinematic variables from capture of 0.5W sized food by H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included timings, duration, velocity, and acceleration of head depression. Head depression distance was the only variable to load heavily on PC 2. brevirostris in the duration and acceleration of lower jaw depression and the times to maximum gape, maximum hyoid depression, onset of lower jaw elevation, and completion of lower jaw elevation. Although there was considerable individual variability both within and among species (F 11,179 = 8.910, p < 0.001), no intraspecific differences were found within N. brevirostris. Variables loading heavily on PC2 for expansive and compressive phase kinematics were the same as those loading heavily for small food items (distances and velocities of lower jaw depression and elevation) (Tables 15, 17). However, the lower jaw of H. francisci moved significantly greater distances and at higher velocities than 140

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141 Table 17. Principal component lo adings of kinematic variable s from 1W feeding trials of H. francisci N. brevirostris and C. plagiosum Expansive & Compressive Variable s PC 1 PC 2 PC 3 PC 4 PC 5 Lower Jaw Depression Distance 0.340 0.768 -0.046 0.239 0.305 Lower Jaw Depression Duration 0.849 0.145 0.262 0.06 0.002 Lower Jaw Depression Velocity -0.309 0.744 -0.265 0.22 0.34 Lower Jaw Depression Acceleration -0.699 0.382 -0.326 0.157 0.196 Time to Maximum Gape 0.920 0.124 0.191 -0.06 0.026 Maximum Gape 0.550 0.484 -0.167 0.198 -0.304 Onset of Hyoid Depression 0.271 -0.067 0.268 0.491 0.518 Time to Maximum Hyoid Depression 0.770 -0.037 0.405 0.203 0.054 Onset of Lower Jaw Elevation 0.768 -0.303 0.189 -0.136 0.094 Lower Jaw Elevation Distance 0.383 0.705 -0.145 0.175 -0.324 Lower Jaw Elevation Duration 0.565 -0.037 -0.628 0.383 -0.115 Lower Jaw Elevation Velocity -0.036 0.825 0.357 -0.118 -0.271 Lower Jaw Elevation Acceleration -0.347 0.594 0.593 -0.248 -0.132 Time to Lower Jaw Elevation 0.874 -0.265 -0.170 0.086 0.015 Head Angle 0.204 -0.061 -0.372 -0.055 -0.462 Protrusion Variables PC 1 PC 2 PC 3 Onset of Protrusion 0.813 0.472 -0.009 Time to Maximum Protrusion 0.863 0.327 0.242 Protrusion Distance -0.607 0.467 0.593 Protrusion Duration 0.301 -0.363 0.828 Protrusion Velocity -0.722 0.642 -0.018 Protrusion Acceleration -0.507 0.561 -0.445 % Gape Reduced -0.544 0.451 0.575 Head Depression Variables PC 1 PC 2 PC 3 Onset of Head Depression -0.794 -0.067 0.575 Time to Maximum Head Depression -0.834 0.390 0.381 Head Depression Distance 0.358 0.912 0.175 Head Depression Duration -0.264 0.861 -0.291 Head Depression Velocity 0.702 0.427 0.476 Head Depression Acceleration 0.414 -0.306 0.726 Bold values indicate vari ables considered to load heavily on a given principal component (loading score > 0.600)

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142 Table 18. Kinematic data 1W feeding trials of H. francisci N. brevirostris and C. Plagiosum Expansive & Compressive Variables H. francisci N. brevirostris C. plagiosum Lower Jaw Depression Dist. (cm) 1.5 0.1 1.1 0.1 0.8 0.0 Lower Jaw Depression Dur. (ms) 52.3 2.0 45.9 1.9 26.6 0.8 Lower Jaw Depression Vel. (cm s -1 ) 29.3 1.3 24.4 1.3 32.5 1.6 Lower Jaw Depression Acc. (cm s -2 ) 687.9 54.9 587.7 48.6 1331.1 87.0 Time to Max Gape (ms) 57.3 2.4 53.9 2.2 28.6 0.8 Max Gape (cm) 3.4 0.1 3.3 0.1 2.0 0.1 Onset of Hyoid Depression (ms) 26.6 1.5 20.1 1.3 19.9 0.7 Time to Max Hyoid Depression (ms) 62.7 2.2 64.9 2.2 46.3 1.1 Onset of Lower Jaw Elevation (ms) 73.1 2.3 87.9 4.2 52.1 2.4 Lower Jaw Elevation Dist. (cm) 1.6 0.1 1.2 0.1 0.7 0.1 Lower Jaw Elevation Dur. (ms) 44.1 2.2 46.9 1.9 29.4 1.5 Lower Jaw Elevation Vel. (cm s -1 ) 41.5 2.6 26.1 1.1 25.7 1.4 Lower Jaw Elevation Acc. (cm s -2 ) 1454.4 176.6 663.1 45.7 1143.5 89.9 Time to Lower Jaw Elevation (ms) 117.2 3.7 134.9 4.6 81.4 2.5 Head Angle ( ) 2.2 0.2 6.6 0.5 1.4 0.3 Protrusion Variables H. francisci N. brevirostris C. plagiosum Onset of Protrusion (ms) 77.9 2.8 90.6 6.6 Time to Max Protrusion (ms) 106.8 3.3 118.6 6.7 Protrusion Dist. (cm) 0.8 0.0 0.5 0.0 Protrusion Dur. (ms) 28.9 1.4 28.1 1.2 Protrusion Vel. (cm s -1 ) 32.7 1.9 18.2 1.2 Protrusion Acc. (cm s -2 ) 1158.2 122.4 765.6 71.7 % Gape Reduced 25.6 1.3 14.3 0.9 Head Depression Variables H. francisci N. brevirostris C. plagiosum Onset of Head Depression (ms) 79.2 3.8 92.2 6.2 63.0 2.8 Time to Max Head Depression (ms) 109.1 4.1 125.5 6.5 90.0 3.3 Head Depression Dist. (cm) 1.1 0.1 0.8 0.1 0.8 0.1 Head Depression Dur. (ms) 29.9 2.8 33.3 2.7 27.0 1.3 Head Depression Vel. (cm s -1 ) 36.8 2.6 23.8 2.0 27.4 1.8 Head Depression Acc. (cm s -2 ) 1437.4 166.3 1743.0 376.9 1119.9 102.6 *Values are means one standard error Acc., Acceleration; Dist., Distance ; Dur., Duration; Vel., Velocity

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Figure 24. Principal components analysis of expansive and compressive phase kinematic variables from capture of 1.0W sized food by H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included timings and durations of lower jaw depression, hyoid depression, and lower jaw elevation, and the acceleration of lower jaw depression. Variables loading heavily on PC 2 included the magnitudes of displacement and velocities of lower jaw depression and elevation. those of both N. brevirostris and C. plagiosum while capturing large food (F 2,179 = 19.948, p < 0.001) (Fig. 24, Table 18). PC3 indicated that lower jaw elevation took significantly less time in H. francisci than in N. brevirostris, both of which were equivalent to C. plagiosum (F 2,179 = 4.088, p = 0.018; Table 17). Although the mean duration of lower jaw elevation by C. plagiosum (29 ms) was lower than those of H. francisci (44 ms) and N. brevirostris (47 ms) (Table 18), considerable intraspecific variability within C. plagiosum precluded its differentiation from H. francisci and N. brevirostris on PC3. Although H. francisci and C. plagiosum had significantly higher 143

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144 factor scores than N. brevirostris on PC5 (F 2,179 = 16.410, p < 0.001), no variables loaded heavily on this axis (Table 17). PCA on palatoquadrate protrusion kinema tics for large food items yielded three axes with eigenvectors greater than 1.0 (86.6% of variance explained). Significant differences were found among species on PCs 1, 2, and 3, and between individuals on PCs 1 and 3. PC1 (F 1,103 = 17.427, p < 0.001) and PC2 (F 1,103 = 12.995, p < 0.001) indicate that palatoquadrate protrusion by N. brevirostris began later, and moved a shorter distance at a lower velocity than in H. francisci (Tables 17, 18; Fig. 25). The only variable that loaded heavily on PC3, on which H. francisci was greater than N. brevirostris (F 1,103 = 8.451, p = 0.004), was protrusion duration (Table 17). This disagrees with the results from small food items, wh ich indicated longer protrusion durations in N. brevirostris This discrepancy is due to a single H. francisci having significantly higher factor scores than four of five N. brevirostris on PC3 (F 8,103 = 3.464, p = 0.001). Although significant intraspecific variability was found on PC1 (F 8,103 = 4.100, p < 0.001) and PC3 (F 8,103 = 3.464, p = 0.001) within H. francisci no intraspecific variability was observed in N. brevirostris PCA on head depression kinematics yielde d three axes with eigenvectors greater than 1.0 (92.3% of variance explained). Head depression occurred earlier and at a higher velocity in H. francisci compared to N. brevirostris, both of which were equivalent to C. plagiosum (F 2,49 = 6.169, p = 0.004; Tables 17, 18). Head depression distance and duration loaded heavily on PC2, while head depression acceleration loaded heavily on PC3 (Table 17).

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Figure 25. Principal components analysis of palatoquadrate protrusion kinematic variables from capture of 1.0W sized food by H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included timings, duration, and velocity of palatoquadrate protrusion. Palatoquadrate protrusion was the only variable to load heavily on PC 2. Effects of Prey Size on Capture Kinematics Significant differences in prey capture kinematics based on prey size were found in H. francisci. PCA on expansive and compressive phase variables for small and large prey yielded five axes with eigenvalues greater than 1.0 (79.6% of variance explained), of which a significant difference was found on PC2 (F 5, 132 = 2.404, p = 0.040). PCA on palatoquadrate protrusion and head depression data both yielded three axes with eigenvalues greater than 1.0, explaining 80.2% and 97.3% of the variance respectively. A significant prey size effect was found on PC2 for palatoquadrate protrusion data (F 3, 128 = 5.963, p = 0.001) and no differences were found for head depression data. Collectively 145

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146 these differences indicated that the lower jaw of H. francisci is depressed farther and at a higher velocity when capturing large prey, resulting in a la rger maximum gape, and that the palatoquadrate is protruded for a longer pe riod of time. No prey size effects were found in either N. brevirostris or C. plagiosum Kinetic Analysis The highest absolute in situ bite force was generated by H. francisci (95 N), followed by C. plagiosum (29 N) and N. brevirostris (13 N). Absolute force duration, times to and away from maximum force, a nd impulse followed the same pattern (Table 19). However, mass-specific bite force and impulse were highest in C. plagiosum (Table 20). Chiloscyllium plagiosum spent the longest amount of time at maximum force (66 ms), followed by H. francisci (44 ms) and N. brevirostris (13 ms). Bite force was applied and released most rapidly by N. brevirostris (470, 550 N s -1 ), followed by H. francisci (300, 457 N s -1 ) and C. plagiosum (249, 208 N s -1 ) (Table 19). The rising slope of the force-time curve was significantly lower than the falling slope in H. francisci ( p = 0.048), Table 19. Kinetic data from bite performance trials of H. francisci N. brevirostris and C. Plagiosum Variable H. francisci N. brevirostris C. plagiosum Max Force (N) 95 13 13 4 29 1 Force Duration (ms) 535 60 114 45 428 189 Time to Max Force (ms) 322 33 46 27 245 118 Time at Max Force (ms) 41 4 13 7 66 37 Time away from Max Force (ms) 212 35 55 19 117 Impulse (kg m s -1 ) 25 6 1 1 8 4 Rising Slope (N s -1 ) 300 34 470 166 249 136 Falling Slope (N s -1 ) 457 65 550 402 208 *Values are means one standard error

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Table 20. Mass-specific kinetic data from bite performance trials of H. francisci, N. brevirostris, and C. Plagiosum Variable H. francisci N. brevirostris C. plagiosum Max Force (N) 0.41 -1.04 0.79 Force Duration (ms) 0.34 -0.59 0.31 Time to Max Force (ms) 0.33 -0.46 0.18 Time at Max Force (ms) 0.20 -0.55 0.44 Time away from Max Force (ms) 0.31 -0.59 0.36 Impulse (kg m s -1 ) 0.39 -0.90 0.63 Rising Slope (N s -1 ) -0.05 -0.29 0.42 Falling Slope (N s -1 ) 0.12 -0.48 0.45 Figure 26. Principal components analysis of kinetic variables from bite performance trials of H. francisci, C. plagiosum, and N. brevirostris. Variables loading heavily on PC 1 included magnitudes and durations of bite force application. Variables loading heavily on PC 2 included maximum bite force and rates of bite force application and release. 147

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148 Table 21. Principal component loadings of bite performance variables of H. francisci, N. brevirostris and C. plagiosum Variable PC 1 PC 2 Maximum Force (N) 0.705 -0.703 Force Duration (ms) 0.983 0.066 Time to Maximum Force (ms) 0.918 0.130 Time at Maximum Force (ms) 0.824 0.074 Time away from Maximum Force (ms) 0.840 0.004 Impulse (kg m s -1 ) 0.940 -0.310 Rising Slope of Force-Time Curve (N s -1 ) -0.497 -0.711 Falling Slope of Force-Time Curve (N s -1 ) -0.220 -0.835 Bold values indicate vari ables considered to load heavily on a given principal component (loading score > 0.600) and equivalent in N. brevirostris and C. plagiosum Time to maximum force was significantly longer than time aw ay from maximum force in H. francisci (P = 0.049), and equivalent in N. brevirostris and C. plagiosum PCA on bite performance data yielded two axes with eigenvecto rs greater than 1.0 (83.6% of variance explained). Significant di fferences were found among species on PCs 1 and 2, and between individuals on PC1. Vari ables that loaded heavily on PC1 were maximum force, force duration, the times t o, at, and away from maximum force, and impulse (Table 21). Heterodontus francisci and C. plagiosum both had significantly higher factor scores on PC1 than N. brevirostris (F 2,56 = 16.831, p < 0.001), indicating that more force is applied over a longer period of time by these sharks, resulting in a greater transfer of kinetic energy (impulse) (Table 19, Fig. 26). Intraspecific differences were found in C. plagiosum on PC1 were (F 11,56 = 3.903, p < 0.001). Negaprion brevirostris had significantly highe r factor scores than H. francisci and C. plagiosum on PC2 (F 2,56 = 25.401, p < 0.001), upon which maximum force, and the rising and falling

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149 slopes of the force-time curve loaded ne gatively (Fig. 26, Table 21). Although species means indicated that bite force was app lied and released at the highest rate by N. brevirostris mass-specific analyses indicated that N. brevirostris performed these behaviors at the lowest rates. Behavioral Canalization Chiloscyllium plagiosum demonstrated the least am ount of variability in expansive phase variables for small and large food items (26.0%, 25.0%). Expansive phase variability was approximately equal in H. francisci (40.6%, 33.1%) and N. brevirostris (41.8%, 40.9%). Chiloscyllium plagiosum also exhibited the least amount of variability in compressive phase variables for small and large food items (32.8%, 35.1%), followed by N. brevirostris (39.0%, 37.3%) and H. francisci (47.4%, 46.4%). Coefficients of variation for palatoquadra te protrusion variables were similar for H. francisci (42.7%, 39.4%) and N. brevirostris (41.6%, 40.2%). Head depression variables again showed that C. plagiosum exhibited the least variable behavior (25.7%, 21.5%). Head depression was variability was comparable in N. brevirostris (39.6%) and H. francisci (40.6%) for small food item s, but much higher in N. brevirostris for large food items (57.2%, 34.0% respectively) The biting performance of H. francisci showed the least variability (32.0%), followed by C. plagiosum (57.1%) and N. brevirostris (87.0%, Table 22).

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150 Table 22. Mean coefficients of variation fo r kinematic and kinetic variable groups in H. francisci, N. brevirostris and C. Plagiosum H. francisci N. brevirostris C. plagiosum 0.5W 1.0W 0.5W 1.0W 0.5W 1.0W Expansive Phase 40.6 33.1 41.8 40.9 26.0 25.0 Compressive Phase 47.4 46.4 39.0 37.3 32.8 35.1 Palatoquadrate Protrusion 42.7 39.4 41.6 40.2 n/a n/a Head Depression 40.6 34.0 39.6 57.2 25.7 21.5 Biting Performance 32.0 87.0 57.1 Discussion Behavioral constraints can afford enhanced performance in accomplishing a subset of ecological tasks while limiting performance in others. The contrasting requirements of ram, suction, and biting in a quatic feeding are manifested in disparate behaviors often rooted in divergent mo rphologies (Van Leeuwen and Muller, 1984; Norton, 1991; Norton and Brainerd, 1993). S ubsequently, numerous kinematic and kinetic differences we re identified among N. brevirostris C. plagiosum and H. francisci sharks that exhibited markedly different pr ey capture behaviors. These data supported predictions of the timings and durations of events during the expansion and compression of the feeding mechanism based upon the relati ve importance of the different phases of the gape cycle in ram, suction, and biting predators. However, numerous pieces of evidence called into question the validity of behavioral predicti ons based on feeding ecology and the mechanics of jaw move ment. The kinematic behaviors of N. brevirostris were highly variable and relatively slow in all aspects of the gape cy cle despite the fact that a rapid compressive phase was hypothesized to be an important characteristic of ram-

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151 feeding. The mass-specific bite force of N. brevirostris was very low, suggesting that factors other than bite force magnitude play a role in its predatory success. Suction feeding in C. plagiosum involved very rapid kinematic behaviors with low variability in all aspects of the gape cycle even though the expansive phase is the primary determinant of suction feeding performance (Sanford a nd Wainwright, 2002; Svanback et al., 2002; Day et al., 2005). The mass-specific bite force of C. plagiosum was also surprisingly high, although its abso lute bite force was relatively low. Heterodontus francisci which captures prey by suction and biting (Edm onds et al., 2001), demonstrated rapid oropharyngeal expansion similar to, though slower than, C. plagiosum The compressive phase kinematics of H. francisci were faster than hypothesized based on the trade-off between force and velocity in mechanical lever systems (Westneat, 1994), and its absolute bite force was mu ch greater than those of N. brevirostris or C. plagiosum indicative of its consumption of hard prey (Fig. 27) (Strong Jr., 1989; Segura-Zarzosa et al., 1997). Ram Feeding Ram feeding by N. brevirostris was characterized by kinematic events that occurred relatively later a nd slower than those in th e suction or suction-biting mechanisms. These findings are intuitive for the expansive ph ase given its lesser importance to ram feeding. Although N. brevirostris depressed its lower jaw faster than many other ram feeding sharks (Trica s and McCosker, 1984; Ferry-Graham, 1997, 1998a; Motta et al., 1997; Wilga and Motta, 1998a, 2000; Motta and Wilga, 2001), as predicted, this behavior was performed slower than in numerous suction feeding sharks

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Figure 27. Representation of kinematic and kinetic behavioral transitions associated with capturing prey via ram, suction, and suction-biting feeding methodologies. Ram is represented by N. brevirostris (upper apex), suction is represented by C. plagiosum (left apex), and suction-biting is represented by H. francisci (right apex). Kinematic changes between each feeding methodology are indicated outside the graded transitional arrow, while kinetic changes are indicated within the graded transitional arrows. 152

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153 (Edmonds et al., 2001; Motta et al., 2002), teleosts (Ferry-G raham et al., 2002b; Sanford and Wainwright, 2002; Day et al., 2005; Gibb and Ferry-Graham, 2005), amphibians (Lauder and Shaffer, 1985; Reilly and Lauder, 1992), and a reptile (Lemell et al., 2002). Relatively long durations, low velocities, and low accelerations of lower jaw depression indicate low inertial forces imparted to the surrounding wa ter, which may account for a lack of suction generation in N. brevirostris (Muller et al., 1982; Motta et al., 1997; Day et al., 2005; D.R. Huber, pers. obs.). Therefore, the slow expansive phase of N. brevirostris may behaviorally constrain it from usi ng suction to effectively capture prey. Additionally, suction feeding is only effective if the predator is close to its prey because suction flow velocity decays exponentially with distance from the mouth (distance -3 ) (Muller et al., 1982; Day et al., 2005). Cons equently, suction is more effective for capturing relatively immobile (easily accessi ble) prey (Ferry-Graham et al., 2002b; Carroll et al., 2004; Gibb and Ferry-Graham, 2005), whereas ram is more commonly used to capture elusive prey (Nort on, 1991; Wainwright et al., 2001). Negaprion brevirostris is an active predator that routinely ram feeds on elusive teleost prey (Cortes and Gruber, 1990; Sundstrom et al., 2001), and as such, its behavior is not su ited for suction prey capture. Contrary to predictions for ram feeding, the compressive phase of N. brevirostris involved relatively late onset s of kinematic events and slow lower jaw elevation. However, hypotheses regarding the compressive phase of ram feeders are based upon the pursuit of elusive prey, which was not pr esented in this st udy. Assuming that N. brevirostris can modulate its prey capture behavior based on prey elusivity (Liem, 1978; Motta et al., 1991; Norton, 1991; Nemet h, 1997a, 1997b; Ferry-Graham, 1998a; Lowry,

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154 2005), the appropriate prey stimuli may e licit a rapid compressive phase. Dietary analyses have shown that N. brevirostris does effectively pursue and capture elusive prey in the wild (Cortes and Gruber, 1990). Additionally, postulating that the compressive phase of N. brevirostris is slow relative to H. francisci and C. plagiosum may be an unjust comparison because suction feeders generally have a more rapid feeding sequence due to synchrony of antagonistic muscle activ ation (Liem, 1978; Lauder, 1980; Alfaro et al., 2001). Nonetheless, lower jaw elevation duration in N. brevirostris was shorter than in other ram feeding sharks (Tricas a nd McCosker, 1984; Ferry-Graham, 1997, 1998a; Motta et al., 1997; Wilga and Motta, 1998a 2000; Motta and Wilga, 2001) and the snapping turtle Chelydra serpentine (Lauder and Prendergast, 1992). Additionally, data from numerous teleosts suggest s that strike velocity is an important determinant of ram feeding success; a hydrodynamic body plan a nd rapid approach to prey may be as important as rapid jaw closure in ram f eeding (Webb, 1984; Ferry-Graham et al., 2001a; Wainwright et al., 2001). Although upper jaw protrusion occurred slowly in N. brevirostris relative to H. francisci it occurred more quickly than in other ram feeding sharks (Tricas and McCosker, 1984; Ferry-Graham, 1997; 1998a; Motta et al., 1997; Wilga and Motta, 1998a, 2000; Motta and Wilga, 2001). Upper jaw protrusion in sharks generally occurs during the compressive phase and significantly reduces lower jaw elevation distance, thereby shortening the compressive phase (M otta et al., 1997; Wilga and Motta, 1998a, 1998b; Edmonds et al., 2001; Dean and Motta, 2004b). Protrusion also reorients the jaws from their hydrodynamic subterminal posi tion, exposing the teeth and allowing for effective biting and manipulating of prey (Springer, 1961; Tricas and McCosker, 1984;

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155 Frazzetta and Prange, 1987; Wilga et al., 2001). In contrast, teleosts exhibit expansive phase jaw protrusion due to mechanical c oupling of the upper ja w to the lower jaw depression mechanism (Alexander, 1967). C onsequently, protrusion mechanisms in sharks generally assist in grasping prey, wher eas those of teleosts generally contribute to expansion of the feeding mechanism during suction feeding (Van Leeuwen and Muller, 1984), although some taxa have capitalized upon expansive phase protrusion for ram feeding (Westneat and Wainwright, 1989; Ferry-Graham et al., 2001a; Konow and Bellwood, 2005). Lower jaw elevation occurred at low accelerations indicating the transmission of relatively little bite force from N. brevirostris to its food, as was found in the biting performance trials. The brief duration of lo w magnitude force (114 ms, 13 N) applied by N. brevirostris and equivalence of the times to a nd away from maximum force and the rising and falling slopes of the force-time curve demonstrate that its biting is characterized by quick, snapping bites. Impul se, as representative of kinetic energy transfer, is minimized by rapidly appl ying low magnitude forces (1 kg m s -1 ). Low impulse generation and relatively slow lower jaw elevation will prevent N. brevirostris from consuming hard-shelled benthic prey, th e composite exoskeletons of which require rapid impact and sustained, high magnitude loading to fracture (P rovan and Zhai, 1985; Christoforou et al., 1989). A pparently little kinetic energy transfer is required for predation by N. brevirostris, perhaps indicating that toot h cutting mechanics play a critical role. However, N. brevirostris likely generates larger b ite forces during natural predation because empirically verified mode ling analyses have shown that 60-70 cm TL N. brevirostris and closely related, ecol ogically similar, ram feeding blacktip sharks

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156 Carcharhinus limbatus generate bite forces of 30-70 N (Frazzetta and Prange, 1987; Hoffmayer and Parsons, 2003; Huber et al ., 2006; Ch. 2). Offering pieces of squid undoubtedly did not elicit maximum bite forces. Physical theory regarding cutting devices and limited empirical evidence provide a basis for interpreting the manner in which the teeth of N. brevirostris cut prey (Frazzetta, 1988; Abler, 1992). The teeth of the lower jaw are sharply pointed and effective at puncturing compliant materials through pressure concentration. Once the tips of the teeth have penetrate d, friction between the teeth a nd the prey will shear the substrate, creating stress concentrations th at lead to material rupture (Frazzetta, 1988; Martin et al., 1998; Motta, 2004). The triangular teeth of the upper jaw will also penetrate via pressure concentration, after which frictio n-based draw cutting takes over (Frazzetta, 1988). As the apical edges of these teeth are forced into the prey, frictional and reaction forces between the teeth and prey cause shear ing and rupture. Furthe r penetration of the teeth causes the substrate to bulge between serrations, converting the draw force acting parallel to the apical edge into a reaction fo rce between the bulged material and the edges of the serrations, further augmenting materi al rupture (Frazzetta, 1988; Motta, 2004). The cutting of prey by N. brevirostris is augmented by lateral head shaking as well, which involves the transmission of force from trunk to the head via a series of sinusoidal muscular waves passed up the body (Frazzetta and Prange, 1987; Motta et al., 1997). Swinging the head from side to side causes th e laterally oriented cusps of the anterior teeth to dig into the prey item, as well as di rect material into the lateral notches of the teeth. Durable connective tissues are severed when they reach this notch because of increased stress concentration (Motta, 2004). Th is interaction between feeding behavior

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157 and dental geometry is why tiger sharks Galeocerdo cuvier are thought to be able to bite through the shells of large sea turtles (Witzell, 1987). Suction Feeding Suction feeding by C. plagiosum was characterized by an extremely rapid kinematic sequence that was 3040% shorter than those of H. francisci and N. brevirostris (Fig. 27). The expansive phase of the gape cycle met with predictions in that C. plagiosum exhibited the shortest duration of lo wer jaw depression, earliest times to maximum gape and maximum hyoid depr ession, and high lower jaw depression velocities and accelerations. Lower jaw depre ssion duration (27 ms), time to maximum gape (28 ms), and time to maximum hyoid de pression (46 ms) occurred as quickly or quicker than in any other sh ark studied to date, and closely matched the timings of kinematic measurements in the ob ligate suction feeding nurse shark Ginglymostoma cirratum (Tricas and McCosker, 1984; Frazzetta and Prange, 1987; Ferry-Graham, 1997, 1998a, 1998b; Motta et al., 1997, 2002; Wilga and Motta, 1998a, 1998b, 2000; Fouts and Nelson, 1999; Edmonds et al., 2001). Maximum hyoid depression occurs 17 ms after maximum gape indicating a rapid posterio rly-directed expansion of the feeding mechanism as well. These expansive phase variables corroborate other studies on suction feeding which indicate that the rate of oropharyngeal expans ion is a key determinant of suction performance in fishes, and as such, has been a primary selective force in the evolution of inertial suction feeding (Laude r, 1980; Muller and Osse, 1984; Van Leeuwen and Muller, 1984; Sanford and Wainwright, 2002; Svanback et al., 2002; Day et al., 2005).

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158 Suction feeding in C. plagiosum is augmented by two sets of tripartite labial cartilages that encircle its mouth. Shortly after the beginni ng of lower jaw depression the labial cartilages swing forward to laterally occlude the gape, maki ng the oral aperture approximately circular. The lower jaw is depr essed a short distance and cranial elevation is relatively non-existent, giving C. plagiosum the smallest maximum gape of the species investigated (Tables 16, 18). Uniformly enci rcling a relatively small gape induces high mainstream velocities in the parcel of wate r being inertially tran sported (Lauder, 1979; Van Leeuwen and Muller, 1984; Norton and Brainerd, 1993). Similar labial configurations and behaviors are found in other suction feeding sharks including H. francisci G. cirratum, leopard T. semifasciata spiny dogfish Squalus acanthias and spotted wobbegong sharks Orectolobus maculatus (Wu, 1994; Ferry-Graham, 1998a; Wilga and Motta, 1998a; Motta and Wilga, 1999; Edmonds et al., 2001; Motta et al., 2002). Anterior maxillary rotation and premax illary translation is an analogous mechanism of lateral gape o cclusion found in suction feedin g teleosts (Alexander, 1967; Lauder, 1979; Muller and Osse, 1984). Unlike teleosts, sharks lack a coupling between the lower jaw depression and upper jaw prot rusion mechanisms, which prevents upper jaw protrusion from contribu ting to suction generation (s ee Dean and Motta (2004b) for exceptions). The hydrodynamic constraints of inducing flow in a viscous medium necessitate lateral occlusion of the gape (Lauder, 1979; Van Leeuwen and Muller, 1984). Thus, suction feeding sharks have evolve d the compensatory mechanism of labial cartilage extension. Although some teleosts have co-opted their upper jaw protrusion mechanism for ram feeding (Westneat a nd Wainwright, 1989; Ferry-Graham et al.,

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159 2001a), the gape occlusion mechanisms of te leosts and sharks are generally not found among true ram feeding taxa (Compagno, 1988; Porter and Motta, 2004) or teleosts that use a biting mechanism to excavate substr ate borne food (Turingan and Wainwright, 1993; Hernandez and Motta, 1997). However, nu merous teleosts and sharks that use a combination of ram and suction do possess gape occlusion mechanisms (Compagno, 1988; Ferry-Graham, 1998a; Wilga and Motta 1998a; Wainwright et al., 2001). Unlike H. francisci G. cirratum and O. maculatus C. plagiosum does not have a terminal mouth. Its labial cartilages are extende d parallel to the ante roventrally oriented jaws, focusing the suction force approximately 45 to the ventral body surface. Because flow velocity induced by suction generation is inversely proportional to the distance away from the mouth (distance -3 ) (Muller et al., 1982; Day et al., 2005), the near-field nature of suction feeding and orientation of the jaws require that C. plagiosum be close to and above its prey, representing both physical a nd morphological constr aints on behavior. Capturing substrate borne prey may facilita te the effectiveness of suction feeding by reducing the effective volume of water in fluenced by pressure generation (Gibb and Ferry-Graham, 2005). However, the lack of a terminal mouth and small gape will inhibit C. plagiosum from successfully ram feeding, excep t perhaps on small elusive benthic prey. Food was generally captured and transporte d to the esophagus in a single gape cycle by C. plagiosum supporting the assertion that the compressive phase is less important to C. plagiosum than to non-suction feeders. Therefore, it would not be surprising to find a protracted compressive phase in C. plagiosum Conversely, the onset and completion of lower jaw elevation occurred earliest in C. plagiosum which had the

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160 shortest durations of lower jaw elevation and total bite time of any shark studied (Tricas and McCosker, 1984; Frazzetta and Pra nge, 1987; Ferry-Graham, 1997, 1998a, 1998b; Motta et al., 1997, 2002; Wilga and Motta 1998a, 1998b, 2000; Fouts and Nelson, 1999; Edmonds et al., 2001). Rapid compression of the feeding mechanism may prevent the escape of elusive prey and is probably due to the rapid synchrony of firing in antagonistic muscle groups in its feeding mechanism, as has been found in numerous suction feeding fishes (Liem, 1978; Lauder, 1980; Alfaro et al., 2001; Mato tt et al., 2005). The high acceleration of lower jaw elevati on indicates a kinematic correlate to the high mass-specific bite force and impulse of C. plagiosum which were greater than those of the other species (Table 19, 20). Impulse is maximized by high bite forces and long durations of force applica tion (Huber et al., 2005), both of which were observed in C. plagiosum These kinetic behaviors may be associ ated with its consumption of benthic crustaceans with a variety of exoskeletal armaments (Compagno, 2001). However, the larger absolute bite forces of H. francisci allow it to consume harder prey including mollusks and echinoderms (Fig. 27) (Strong Jr., 1989; Segura-Zarzosa et al., 1997). Suction-Biting Despite having a high bite force (Taylo r, 1972; Summers et al., 2004; Huber et al., 2005), similar to other predators of sessile benthic invertebrates H. francisci initially captures prey using inertial suction (Edm onds et al., 2001; Ferry-Graham et al., 2002b; Carroll et al., 2004; Gibb and Ferry-Graham, 2005). Several characteristics of its expansive phase consequently mirror those of C. plagiosum Heterodontus francisci generally had intermediate values in the va riables describing the e xpansive phase of the gape cycle (Fig. 27). The lower jaw was depr essed at a high veloci ty and maximum hyoid

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161 depression followed maximum gape by only 511 ms, indicating a rapid, posteriorly directed abduction of the feeding mechanism. Unlike C. plagiosum maximum hyoid depression occurred late in the kinematic sequence indicating that hyoid-mediated expansion of the feeding mechanism occurred at a slower rate in H. francisci Large lower jaw depression gave H. francisci a maximum gape comparable to N. brevirostris without a major contribution from cranial el evation. A large, terminal gape affords H. francisci the ability to capture large prey item s such as sea urchins, which may be dislodged from the substrate via rapid upper jaw protrusion, as hypothesized by Edmonds et al. (2001). However, a large gape may re duce its suction pressure because the generated force is distributed over a la rge buccal area. The expansive phase of H. francisci exhibits characteristics that both augm ent (high lower jaw depression velocity, labial cartilage extension) and detract from (low rate of hyoid depression, large gape) suction generation (Muller et al., 1982; Motta et al., 2002; Day et al., 2005). These morphological and behavioral constraints represent func tional compromises between suction and biting. Given that the consumption of hard prey re quires large bite forces and that force and velocity are inversely proportional in mechanical lever systems (Westneat, 1994; Wainwright and Shaw, 1999), the compressive phase of H. francisci was hypothesized to be relatively slow. Contrarily, lower ja w adduction and palatoquadrate protrusion occurred relatively early and rapidly. Unexp ectedly rapid biting kinematics have recently been observed in several labrid fishes as well (Gibb and Ferry-Graham, 2005). Times to the onset, completion of, and durat ion of lower jaw elevation in H. francisci were intermediate amongst the three species, while velocities and accelerations of lower jaw

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162 elevation and upper jaw protrusion were the hi ghest. Although the rapid nature of these events may represent the synchrony of an tagonist muscle activity found among suction feeders (Liem, 1978; Lauder, 1980; Alfaro et al., 2001; Matott et al., 2005), the high velocities and accelerations are in dicative of high kinetic energy transfer from predator to prey. The majority of prey consumed by H. francisci are sessile (Strong Jr., 1989; Segura-Zarzosa et al., 1997), ruling out the ro le of entrapping elusive prey within the jaws as a motivating factor for rapid co mpressive phase kinematics. Palatoquadrate protrusion and lower jaw elevat ion reach their maximum excu rsions within 7-10 ms of each other, causing a nearly simultaneous impact of both jaws on a prey item. This will induce large stresses in prey because movement of the item due to impact with one jaw is resisted contralaterally by the other jaw. Th ese findings support the assertion of Edmonds et al. (2001), who proposed that the upper jaw of H. francisci may be used as a tool to chisel at substrate-affixed prey. The high velocities and accelerations of the compressive phase translated into large kinetic energy transfer by H. francisci which had the highest absolute bite force and impulse. Applying high magnitude, l ong duration forces maximizes impulse generation by increasing bite force output pe r unit time. These kinetic behaviors increase the amount of energy contributing to the fracture of prey w ith composite exoskeletons like sea urchins, which are composed of calci te ossicles linked by collagenous ligaments (Ellers et al., 1998). Sustained loading after a high velocity impact effectively fractures composites because they harden to a satu ration point upon initial compression. Sustained loading after this initial compression induces crack nucleation, followed by structural failure (Provan and Zhai, 1985; Christoforou et al., 1989). Cyclic al bite force application

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163 observed in H. francisci will further augment the fracture of composite exoskeletons because the rate at which th e strength of a composite structure degrades is a power function of the number of stra in cycles to which it is subjected (Hwang and Han, 1989; Huber et al., 2005). Multiple force peak s within a given bite indicate that H. francisci may have evolved motor patterns specialized for consuming hard prey, which have also been found in other durophagous fi shes including the bonnethead shark Sphyrna tiburo (Bemis and Lauder, 1986; Turingan and Wainwright, 1993; Wilga and Motta, 2000). Variability in Prey Capture Behavior The occurrence of interand intraspeci fic variability has been a hallmark of comparative studies on vertebrate feedi ng (Wainwright and Lauder, 1986). While interspecific variability is expected among taxa utilizing different methodologies for a given task, the breadth of variability with in a species is indicative of behavioral constraints on performance. Chiloscyllium plagiosum exhibited lower variability in all kinematic behaviors than H. francisci and N. brevirostris Because suction generation is contingent upon rapid, posteriorly direct ed abduction of the feeding mechanism, variability in these behaviors would likel y compromise performance (Sanford and Wainwright, 2002; Svanback et al., 2002). Both kinematic and electromyographic analyses have demonstrated limited vari ability in the oblig ate suction feeder G. cirratum as well (Motta et al., 2002; Matott et al., 2005). It was ther efore surprising that the expansive phase of H. francisci which initially uses suction to capture prey (Edmonds et al., 2001), was relatively variable. The bimodal prey capture behavior of H. francisci may constrain its suction behavior because its feeding mechanism is primarily designed for biting (high mechanical advantage, hypertr ophied jaw adductors, r obust jaws, molariform

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164 teeth) (Nobiling, 1977; Summers et al., 2004; Huber et al., 2005). Heterodonts francisci was surprisingly variable in compressive phase kinematics in light of the contingency of hard prey consumption upon jaw adduction. The sh ear magnitude of its bite force and the lack of elusive prey in its diet may afford it this behavioral flexibility. The breadth of expansive and compressive phase behaviors exhibited by N. brevirostris in this study (high coefficients of variability but no intraspecific differences) may allow it to effectively encounter and apprehend a wide range of prey. Variability in biting performance told a different story than that of cranial kinematics. Coefficients of va riability were very low in H. francisci relative to C. plagiosum and N. brevirostris. This low variability is associ ated with consistent kinetic energy transfer and, in general, an effectiv e bite force delivery mechanism. Conversely, the extremely variable biting performance of N. brevirostris may be attributed in part to the importance of dental cutt ing mechanics to its predatory behavior, not the magnitude of kinetic energy transfer from its jaws to prey. Behavioral motivation may have played a role in the low kinetic energy magnitudes measured however. Provided that low variability in kinetic parameters and consis tent kinetic energy transfer are valuable commodities in eating hard prey, th e intermediate variability of C. plagiosum parallels its consumption of prey of vary ing hardness, ranging from bony fishes to crustaceans (Compagno, 2001). Collectively, these patterns of kinematic and kinetic variability demonstrate that taxa using the jaws to perform specialized ta sks (suction generation, crushing hard prey) exhibit less variability in the behavioral variables most relevant to those tasks (i.e. increased precision (Fe rry-Graham et al., 2002a)).

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165 Conclusions Behavioral constraints, which are often a manifestation of morphological diversity, are a primary determinant of eco logical breadth and performance. Given a constraint, the subset of possi ble behaviors at an organism s disposal determines its proficiency at a range of ecologically relevant tasks and likely influences the decision to engage in certain tasks. The crania l kinematics and bite performance of N. brevirostris C. plagiosum and H. francisci demonstrated numerous attri butes that both augment and constrain their abilities to perform ram, suction, and biting. The large gape, slicing dentition, and extensive upper jaw protrusion of N. brevirostris are ideal for using ram feeding to capture elusive prey. However, slow jaw movements and low bite forces will limit its ability to generate suction and cr ush hard prey. Although the extremely rapid expansion of the feeding mechanism, la bial cartilage extension, and small, anteroventrally directed gape of C. plagiosum will facilitate benthic suction feeding, the small gape, a consequence of both behavioral and morphological cons traints, will also inhibit it from capturing large elusive prey. Despite having th e highest mass-specific bite force of the three sharks, the absolute bite force of C. plagiosum will ultimately limit its ability to consume hard prey as well. Lastl y, the large gape, high bite force, molariform teeth, and repeated compressions of the jaws prior to deglutition will assist H. francisci in crushing large, hard prey items. Its relati vely slower expansion of the oropharyngeal region and large, terminal gape of H. francisci may limit the magnitude of suction pressure it can generate, however. Collectivel y, this investigation has provided evidence for the manner in which behavior can influence feeding ecology and has elucidated specific behavioral attributes and constraints associated with ram, suction, and biting in

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166 sharks, from which the general selective pr essures influencing th eir evolution can be inferred.

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167 Chapter 5: Comparative Prey Capture Biom echanics of Sharks: Implications for the Evolution of Jaw Suspension Mechanisms Abstract The major trend in the evolution of el asmobranch feeding mechanisms has been progressively enhanced kinesis of the jaws re lative to the cranium. This enhanced kinesis has been facilitated by reducti on of the size and number of the articulations between the jaws and cranium during the evolutionary transition from amphist ylic to hyostylic, orbitostylic, and euhyostylic jaw suspension m echanisms. Subsequent to this transition, greater protractility of the jaws brought about the diversification of elasmobranch feeding mechanisms into the ram, suction, biting, and filter feeding mechanisms of extant species. The mechanical consequences of this evolut ionary transition were investigated through biomechanical modeling of the feeding mechanis ms of an amphistylic species (sharpnose sevengill Heptranchias perlo) and three hyostylic species (lemon Negaprion brevirostris whitespotted bamboo Chiloscyllium plagiosum and horn Heterodontus francisci ) representing the ram, sucti on, and biting mechanisms. The results indicate that the ancestral suspensorial loading pattern i nvolved compression at the anterior craniopalatine articulation and tens ion at the posterior hyomandibul ar articulation. Suspensorial loading increased in magnitude with the deve lopment of muscular forces (preorbitalis) acting between the jaws and cranium. Additi onally, reversal of th e ancestral loading regime occurred when the jaws became protrusible enough to dissociate from the anterior

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168 cranio-palatine articulation, as in N. brevirostris and the batoid elasmobranchs. Mechanical modeling was used to identify trends in the functional diversification of the feeding mechanisms of these sharks as well. Modest correlations we re identified between the mechanics of jaw and hyobranchial abduc tion and the ability to generate suction during feeding. The mechanics of jaw adduction and bite forces were more indicative of the feeding ecology of the four species. Th eoretical maximum bite force ranged from 92 245 N in H. perlo, 128 321 N in H. francisci, 69 127 N in C. plagiosum and 69 217 N in N. brevirostris

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169 Introduction The elasmobranch fishes (sharks, skat es, and rays) are a highly diverse group of primarily marine predators that first arose in the late Ordovician period, approximately 450 million years ago (Janvier, 1996; Turn er, 2004). These basal cladodont level elasmobranchs underwent several major radi ations including th e evolution of the hybodontoids (late Carboniferous/early Permia n period, approx. 300 m.y.a.), which were the dominant elasmobranchs of the early Mesozoic, and culminating in the evolution of modern neoselachian elasmobranchs (late Pe rmian/early Triassic period, approx. 250 m.y.a.), which became dominant in the late Mesozoic and remain so today (Moy-Thomas and Miles, 1971; Carroll, 1988). A major trend in the evoluti on of elasmobranch feeding mechanisms has been the movement of the mouth from a terminal to a sub-terminal position and enhanced kinesis of the jaws relative to the cranium. The success of these fishes is believed to be predicated, in part, upon the highly protractile nature of their jaws, which can be protruded up to 100% of an animals head length in modern forms (Schaeffer, 1967; Dean and Motta, 2004b). This remarkable kinesis is due to the independent nature of the musculoskeletal at tachments between their jaws and cranium. Unlike their sister-taxa the holocephalans, the upper jaws of elasmobranchs do not fuse to the cranium (Grogan et al., 1999). Rather, the posterior margins of the jaws articulate indirectly with the otic region of the cranium via hyomandibular cartilages and postorbital, orbital, or ethmoidal articulati ons between the upper jaw and cranium may be present as well (Fig. 28) (Gregory, 1904; Ma isey, 1980; Wilga, 2002). The mechanical consequences of anatomical ch anges that have led to this remarkable performance have rarely been investigated quantitat ively however (Huber et al., 2005).

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Figure 28. Right lateral views of the feeding mechanisms of elasmobranchs with different jaw suspensions. A) Cladodont level Cladodus (amphistyly); B) Hybodont level Hybodus (amphistyly); C) sharpnose sevengill shark Heptranchias perlo (amphistyly); D) horn shark Heterodontus francisci (hyostyly); E) whitespotted bamboo shark Chiloscyllium plagiosum (hyostyly); F) lemon shark Negaprion brevirostris (hyostyly); G) lesser electric ray Narcine brasiliensis (euhyostyly). C, ceratohyal; CR, cranium; E, ethmoidal articulation; H, hyomandibula; LJ, lower jaw; O, orbital articulation; PO, postorbital articulation; UJ, upper jaw. Cladodus, Hybodus, and N. brasiliensis were redrawn from Schaeffer (1967), Maisey (1982), and Dean and Motta (2004a). 170

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Figure 29. Dorsal views of the neurocrania of the A) cladodont shark Cladodus, B) sharpnose sevengill shark Heptranchias perlo, and C) shortfin mako shark Isurus oxyrinchus, illustrating the reduction of the postorbital processes during the evolutionary transition from amphistyly to hyostyly. PO, postorbital process. Cladodus, H. perlo, and I. oxyrinchus were redrawn from Schaeffer (1967) and Daniel (1934). All cladodont level elasmobranchs had an amphistylic jaw suspension in which the large otic process of the upper jaw articulated with, and was ligamentously suspended from, the laterally expanded postorbital process of the cranium (Figs. 28, 29). This anatomical constraint severely limited kinesis of the upper jaw relative to the cranium (Schaeffer, 1967; Maisey, 1980; Wilga, 2002). The palatine portion of the upper jaw was buttressed against and ligamentously suspended from the ethmoid region of the cranium and a pair of long hyomandibular cartilages was present as well. The hyomandibular cartilages of these sharks were non-suspensory, reflecting their ancestry from a post-mandibular visceral arch (Moy-Thomas and Miles, 1971; Zangerl and Williams, 1975; Maisey, 1980; Mallatt, 1996). Early hybodont level elasmobranchs retained an amphistylic jaw suspension (Schaeffer, 1967; Moy-Thomas and Miles, 1971), although the otic process of the upper jaw was significantly reduced in later taxa, such that it no 171

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172 longer articulated with the posto rbital process of the cranium ( Asteracanthus Hybodus Tribodus (Peyer, 1946; Maisey, 1980, 1982, 1987; Ma isey and de Carvalho, 1997)). Loss of the postorbital articulation was associated with an enlargement of the ethmoidal articulation and an increase in the size a nd suspensorial role of the hyomandibular cartilages in these late hybodontoids. Collect ively these changes permitted enhanced jaw kinesis relative to cladodont and early hybodont elasmobranchs (Maisey, 1982, 1987; Maisey and de Carvalho, 1997). The hexanchiform (sixgill, sevengill, and frill) sharks are the only extant elasmobranchs to have retained an amphistylic jaw suspension, featur ing an orbital, not ethmoidal articulation between the palatine process of the upper jaw and the orbital region of the cranium. The hyomandibular cartilages of these sharks are also nonsuspensory (Fig. 28) (Daniel, 1934; Compagno, 1977; Wilga, 2002). All other neoselachians evolved one of three variants of the hyostylic jaw suspension in which the hyomandibular cartilages became the primary supportive elements between the jaws and cranium. This was accomplished by reductions of the otic and postorbital processes of the upper jaw and cranium respectively, such that these structures no longer contacted, and enlargement of the hyomandibulae (Fig. 28) (Gregory, 1904; Maisey, 1980; Cappetta, 1987; Wilga, 2002). Enlargement of the hyom andibulae, presumably indicative of enhanced load-bearing ability, and reduction of the otic process convergently evolved in late hybodontoids and neoselachians (Maisey and de Carvalho, 1997). However, the late hybodontoids were functionally amphistylic due to retained contact between the upper jaw and postorbital region of the cranium (Schaeffer, 1967; Maisey, 1982).

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173 Hyostyly in the traditional sense evolved in the galeomorph sharks (heterodontoids, orectoloboids, lamnoids, and ca rcharhinoids) and is characterized by the presence of a suspensory hyomandibula a nd an ethmoidal articulation (Compagno, 1977; Maisey, 1980; Wilga, 2002). Orbitostyly is a variant of hyostyly found in the squalomorph (hexanchoids, squaloids, and pristiophoroids) and squatinomorph (squatinoids) sharks, in which the palatine pr ocess of the upper jaw articulates with the orbital region of the cranium, not th e ethmoid region (Compagno, 1977; Maisey, 1980; Wilga, 2002). Lastly, euhyostyly is found in the batoids (skates and rays) and is characterized by the lack of anterior cr anio-palatine connections such that the hyomandibular cartilages are the sole structur es suspending the jaws from the cranium (Gregory, 1904; Wilga, 2002). Euhyostyly gene rally involves the dissociation of the hyomandibular cartilages from the other elements of the hyoid arch, creating a mechanism in which the jaws and hyomandibul ar cartilages can be freely pivoted about the cranio-hyomandibular artic ulation (Fig. 28) (Miyake a nd McEachran, 1991; Dean and Motta, 2004a). The transitions from amphistyly to hyostyly and orbitostyly, and from hyostyly/orbitostyly to euhyostyly involved lo sses of the postorbital articulation and eventually the anterior liga mentous attachment between the upper jaw and cranium. The phylogenetic position of the batoids is unres olved due to contrasting morphological and molecular analyses (Shirai, 1992, 1996; Doua dy et al., 2003; Winchell et al., 2004), so it cannot be determined whether euhyostyly arose from hyostyly or orbitostyly. Nonetheless, decoupling of skeletal elements increases the degrees of freedom in a system, consequently increasing the diversity of forces to which those elements are

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174 subject (Herrel et al., 2000). However, there is mixed sentiment regarding the degree of functional consequence that changes in jaw suspension had on jaw kinesis because of widely varying magnitudes of upper jaw protru sion within taxa sharing the same jaw suspension type (Wilga, 2002). This lack of a predictive relationship between jaw suspension type and the exte nt of upper jaw protrusion in confounded by the geometry and activity patterns of the muscles involved in jaw kinesis as well (Wilga et al., 2001; Wilga, 2005). In fact, the expectation that all elasmobranchs with a given jaw suspension will have comparable upper jaw protrusion is unwarranted due to this muscular diversity. Disregarding the nuances of protrusion with in individual species, it appears that the evolutionary progression towards increased kinesis of the jaws relative to the cranium has been associated with both a reduction in th e size and number of articulations between the upper jaw and cranium, and diversification in the size and nu mber of muscles actuating protrusion (Schaeffer, 1967; Moss, 1972; Mais ey, 1980; Liem et al., 2001; Wilga, 2002, 2005). Although some descriptions have alleged that the postorbital articulation of amphistylic hexanchiform sharks will pr eclude upper jaw kinesis (Schaeffer, 1967; Zangerl and Williams, 1975; Wolfram, 1984), li mited protrusion has been observed in the broadnose sevengill shark Notorynchus cepedianus (Wilga, 2002). Short ethmopalatine ligaments and the inabil ity of the upper jaw to disengage from its orbital articulation with the cranium are thought to limit protrusion in these sharks (Compagno, 1977; Wilga, 2002). In contrast, the jaws of numerous hyostylic species are highl y protrusible and can significantly reduce the time and distance re quired to close the jaws (Tricas and McCosker, 1984; Wu, 1994; Motta et al., 1997; Ferry-Graham, 1998a). However, the

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175 tight association between th e upper jaw and cranium in so me hyostylic he terodontiform and orectolobiform sharks apparently limits protrusion (Wu, 1994; Edmonds et al., 2001). Large protrusion has also been observed in S. acanthias, the only orbitostylic shark in which protrusion has been measured (Wilga and Motta, 1998a). The greatest degree of upper jaw protrusion is afforded by the batoid euhyostylic jaw suspension due to the lack of anterior cranio-palatine attachments. The lesser electric ray Narcine brasiliensis is capable of protruding its jaws 100% of its h ead length, as well as asymmetric protrusion (Dean and Motta, 2004b). The enhanced jaw kinesis afforded by changes in jaw suspension is believed, in part, to have increased the f unctional versatility of the feed ing mechanism, resulting in the ram, suction, biting, and f ilter feeding mechanisms of mo dern elasmobranchs (Moss, 1977; Motta, 2004). This diversification is indicated throughout the fossil record by dentitions specialized for gr asping, tearing, slicin g, crushing, and grindi ng, and is evident in the gross cranial morphology of modern forms (Zangerl, 1981; Cappetta, 1987; Motta, 2004). Based upon the historic transformations that have occurred in elasmobranch jaw suspension mechanisms, the primary objective of the present study was to identify the mechanical consequences of the transition from amphistyly to hyostyly by modeling the forces occurring throughout the jaws and thei r articulations with the cranium in sharks representing amphistyly (sharpnose sevengill Heptranchias perlo), hyostyly with a nondisarticulating upper jaw (horn Heterodontus francisci whitespotted bamboo Chiloscyllium plagiosum ), and hyostyly with a disa rticulating upper jaw (lemon N. brevirostris ) (Daniel, 1934; Motta and Wilg a, 1995; Wilga, 2002). At maximum protrusion the upper jaw of N. brevirostris rotates far enough away from the cranium that

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176 contact at the ethmoidal arti culation is lost (Motta and Wilga, 1995). An orbitostylic species was not included in this analysis b ecause the orbital proce ss is not capable of disarticulating from the cranium in the speci es that have been investigated (Compagno, 1977; Wilga and Motta, 1998a). Therefore, orbitostyly is considered functionally analogous to hyostyly with a non-disartic ulating upper jaw. To investigate the diversification of elasmobranch feeding m echanisms associated with the increased functional versatility of their jaw suspensi ons, the secondary objective of this study was to relate the magnitudes and orientations of the forces produced by the cranial musculature and the loadings acting on cranial elements in H. francisci N. brevirostris C. plagiosum and H. perlo to the prey capture met hodologies of these sharks. Materials and Methods Species Descriptions Heterodontus francisci uses suction and/or biting to capture prey, which is grasped by the anterior cuspidate teeth and th en crushed by the posterior molariform teeth (Strong Jr., 1989; Edmonds et al ., 2001; Huber et al., 2005). Negaprion brevirostris is a ram feeder with piercing and slicing teeth that routinely uses ja w protrusion and headshaking to bite and slice through elusive pr ey (Frazzetta and Prange, 1987; Cortes and Gruber, 1990; Motta et al., 1997). Chiloscyllium plagiosum is a suction feeder with small, cuspidate teeth that consumes a variety of bony fishes and crustaceans (Compagno, 2001; Lowry, 2005). Although the feeding behavior of H. perlo has not been directly quantified, limited dietary analyses as well as dental and cranial morphology suggest that it ram captures elusive prey, which it pierces with fang-like upper teeth and cuts with

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177 multi-cuspidate lower teeth (Bigelow and Schroeder, 1948; Schaeffer, 1967; Compagno, 1984a). Theoretical maximum force generati on in the cranial musculature of H. francisci ( = 63 cm TL, n = 5), N. brevirostris ( = 66 cm TL, n = 4), C. plagiosum ( = 66 cm TL, n = 4), and H. perlo sharks ( = 77 cm TL, n = 4) was determined in order to develop biomechanical models of prey capture. Specimens of approximately the same length were used to minimize size effects. Fresh dead specimens of H. francisci and N. brevirostris were obtained off the coasts of Los Angeles, CA and Miami, FL respectively, while C. plagiosum was obtained from SeaWorld Advent ure Park in Orlando, FL. Preserved specimens of H. perlo were acquired from the Florida Mu seum of Natural History at the University of Florida (catalog numbers UF 38553, UF 78000, and UF 112211). Morphological Analysis The positions of the origins and inse rtions of cranial muscles involved in expanding and compressing the feeding mechanis ms were estimated using the tip of the snout as the origin of a three-dimensional coordinate system (Table 23, Fig. 30). Muscles with multiple heads were separated into their constituent portions and positional data was collected for individual muscle heads. Diffi culty in separating the six heads of the quadratomandibularis-preorbitalis complex in H. francisci led to their analysis as a group. Positional data were collected by measuring the distance of the origins and insertions from the respective X, Y, and Z planes intersecting the tip of the snout. Each muscle was then excised (unilaterally where applicable ), bisected through its center of mass perpendicular to the principal fiber direction, and digital im ages of the cross-sections were taken. Cross-sectional ar eas were measured from these images using Sigma Scan

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Figure 30. Coordinate system for three-dimensional vector analysis of the forces generated by the cranial musculature represented by H. francisci. Directionality is defined with respect to the head using the right-hand rule. Pro 4.01 (SYSTAT Software Inc., Point Richmond, CA, USA). Center of mass was estimated by suspending the muscle from a pin and tracing a vertical line down the muscle. After repeating this from another point, the intersection of the two line-tracings indicated the center of mass, through which the muscle was bisected. Due to stipulations of the museum loan, data were not collected for muscles involved in the expansion of the feeding mechanism of H. perlo. The three-dimensional coordinates of the center of rotation of the quadratomandibular jaw articulation, ethmoidal articulation between the palatal region of the upper jaw and chondrocranium, and the lateral and medial articulations of the hyomandibula with the jaws and chondrocranium respectively were determined with respect to the right side of the head of each individual. Points corresponding to 0 and 178

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179 100% of the distance along the functional tooth row on the lower jaw from the posteriormost tooth were also determined; 100% is the anterior-most tooth. In-levers and outlevers for lower jaw abduction and adduc tion were determined from the threedimensional coordinates of the muscles a nd points on the jaws in order to estimate mechanical advantage ratios for the opening a nd closing of the jaws. The in-lever for jaw abduction was the distance from the center of ro tation of the jaw joint to the insertion of the coracomandibularis on the lower jaw. In -levers for each jaw adducting muscle were the distances from the center of rotation of the jaw joint to the origin of each muscle on the lower jaw. A weighted average of the a dductive in-levers was determined based on the forces produced by their respective musc les. The abductive and weighted adductive in-levers were divided by the out-lever dist ance from the center of rotation of the jaw joint to the tip of the anterior-most tooth of the lower jaw to determine mechanical advantage ratios for jaw abduction and adductio n (Fig 31a). Mechanical advantage ratios indicate the trade-off between force and velocity in lever systems, with high values indicating force efficient systems and low va lues indicating velocity efficient systems (Westneat, 1994). A mechanical advantage ratio for jaw adduction at the posterior margin of the functional tooth row was determined in this way as well. Anatomical nomenclature is based on Daniel (1915, 1934), Goto (2001), Motta and Wilga (1995, 1999), and Nobiling (1977). Theoretical Force Generation Cross-sectional area (A CS ) measurements of the muscles were multiplied by the specific tension (T SP ) of elasmobranch white muscle (289 kN/m 2 (Lou et al., 2002)) to determine the theoretical maximum tetanic force (P O ) of each:

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180 P O = A CS T SP Force vectors for each muscle were then constructed from their maximum tetanic forces and the three-dimensional coordinates of their origins and insertions. The force vectors of muscles excised unilaterally were reflected about the Y-plane to represent the forces generated by the musculature on the other side of the head. Mathcad 11.1 software (Mathsoft, Inc., Cambridge, MA, USA) was used to model the static equilibrium of the feeding mechanisms during jaw abduction a nd adduction in each species. The moments generated by the adductive musculature about the jaw joints were us ed to determine the theoretical maximum bite force and resulting jaw joint reaction forces for each individual (F B F JR Fig. 31b). Maximum bite force was modeled at points 0 and 100% of the distance along the functional tooth row from the posteri or-most tooth. Theoretical estimates of maximum bite force have been shown to be accurate predictors of tetanically stimulated maximum bite force in H. francisci C. plagiosum and the spiny dogfish Squalus acanthias (Huber and Motta, 2004; Hube r et al., 2005; Ch. 3). Mechanical loading at the ethmoidal and hyomandibular articulations of the jaws with the chondrocranium and hyomandibular car tilages respectively were determined for bites occurring at 0% and 100% of the distance along the functional tooth row. Summation of moments from muscular fo rces acting on the upper jaw about the ethmoidal articulation was used to determ ine the force acting at the hyomandibular articulation (F H Fig. 31b). The hyomandibula was modeled as a two-force member, moveable about its articulati ons with both the upper jaw a nd chondrocranium (Hibbeler, 2004). The force acting through the hyomandibula was then determined from its threedimensional orientation and the force acting at its articulation with the jaws. The force

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Figure 31. Schematic diagram of the jaws of N. brevirostris indicating (A) variables for mechanical lever-ratio analysis, (B) forces involved in the static equilibrium calculations of the lower and upper jaws, and (C) the disarticulation of the upper jaw from the cranium at maximum upper jaw protrusion (redrawn from Motta and Wilga (1995)). AB, resolved in-lever for jaw adduction; AC, out-lever; BD, resolved adductive muscle force vector; F B bite reaction force; F E reaction force at the ethmoidal articulation; F H reaction force at the hyomandibular articulation; F JR jaw joint reaction force; F PO force generated by the preorbitalis; F QM force generated by the quadratomandibularis; P 0 maximum tetanic tension. Arrow size does not indicate force magnitude. 181

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182 acting at the ethmoidal articulation was subsequently determined from static equilibrium calculations of the upper jaw (F E Fig. 31b). The postorbital articulation between the upper jaw and cranium in H. perlo readily disengages during protrusion (Compagno, 1977; Wilga, 2002), and so contact at this point was not included in the modeling analysis. Additionally, the moment acting on the lower jaw during jaw opening via the coracomandibularis muscle was used to determine theoretical maximum jaw opening forces in H. francisci N. brevirostris and C. plagiosum Protrusion of the upper jaw during prey capture by N. brevirostris involves the disarticulation of the upper jaw from the chondrocranium, precluding loading at the ethmoidal articulation (Fig. 31c) (Motta and Wilga, 1995). To account for this condition, a second model of the upper jaw was develope d in which loading at the hyomandibular articulation is determined directly from the static equilibrium of the upper jaw. This model included the force generated by the levator palatoquadrati muscle in N. brevirostris which is associated with the deri ved upper jaw protrusion mechanism of carcharhinid sharks (Compagno, 1988; Wilga et al., 2001). Changes in the positions of the musculoskeletal elements during jaw prot rusion were not accounte d for in the static equilibrium models. Upper jaw kinesis will slig htly modify the relative three-dimensional orientation of components in the feeding m echanism, which can affect the estimated maximum bite force (Herrel et al., 2000). Statistical Analyses All mechanical advantage ratios, muscle forces, and bite forces were compared among species using one-way ANOVA ( p = 0.05) and all significant differences were investigated post-hoc with Tukeys pairwise compar isons test. Principal components

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183 analysis (PCA) based on a corr elation matrix of jaw adductin g muscle forces, mechanical advantages, and the resulting force dist ributions throughout the jaws and their articulations with the cranium was used to identify covariatio n in biomechanical variables. Variables with factor scores grea ter than 0.6 were consid ered to load heavily on their respective principal components (PCs). All statistical analyses were performed in SYSTAT 10 (SYSTAT Software In c., Point Richmond, CA, USA). Results In general, the jaw and hyoid abducting musculature generated more force in suction feeding H. francisci and C. plagiosum than in the ram feeding N. brevirostris although these differences were only partially supported by st atistical analyses (Table 23). The coracomandibularis of H. francisci generated significantly more force than that of N. brevirostris (F 2,10 = 4.792, p = 0.035), while the co racoarcualis of C. plagiosum generated significantly more force than that of N. brevirostris (F 2,10 = 5.803, p = 0.028). Surprisingly, no statistical differences were found in the force produced by the primary hyoid arch abductor, the coracohyoideu s. The coracobranchiales of both H. francisci and N. brevirostris generated more force than that of C. plagiosum (F 2,10 = 18.223, p < 0.001). The jaw opening mechanical advantages of H. francisci N. brevirostris and C. plagiosum were equivalent as well (Tables 23, 24) Due to the larger force produced by the coracomandibularis of H. francisci and the equivalent jaw opening mechanical advantages of H. francisci and N. brevirostris the resultant ja w opening force of H. francisci was greater than that of N. brevirostris (F 2,10 = 8.948, p = 0.006) (Table 24).

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184 Table 23. Bilateral forces (N) produced by cranial muscles during the expansion and compression of the feeding mechanisms of H. francisci N. brevirostris, C. plagiosum and H. perlo Muscle H. francisci N. brevirostris C. plagiosum H. perlo Coracoarcualis (E) 87 4 ab 63 7 b 96 17 a Coracobranchiales (E) 107 8 a 148 11 a 36 7 b Coracohyoideus* (E) 57 4 a 51 6 a 58 8 a Coracomandibularis* (E) 31 5 a 13 2 b 23 4 ab Preorbitalis (C) 52 5 a 50 4 ab 56 7 a 22 4 b Quadratomandibularis (C) 324 20 a 182 4 b 134 21 b 309 36 a Levator Palatoquadrati (C) 89 8 exp active during expansive phase; co mp active during compressive phase Superscript letters denote significant differences fr om statistical analyses Unpaired muscles along longitudinal axis do not produce force "bilaterally" Forces produced by the jaw adducting musc ulature were more indicative of the prey capture me thodologies of H. francisci N. brevirostris, C. plagiosum and H. perlo than those produced by the abducting musc ulature. The quadratomandibularis of H. francisci and H. perlo, which rely upon crushing sedent ary and grasping elusive prey between their jaws respectively, generated significantly more force than those of N. brevirostris and C. plagiosum which bite/slash and suction capture their respective prey (F 3,12 = 20.069, p < 0.001). The forces generated by the preorbitalis of H. francisci and C. plagiosum were greater than that of H. perlo (F 3,12 = 5.044, p < 0.022), all of which were equivalent to N. brevirostris (Table 23). The principal co mponent of the adductive force vector was oriented vertically in H. perlo, H. francisci and C. plagiosum and represented 91%, 70%, and 60% of the ge nerated adductive force respectively. Conversely, the principal component of the adductive force vector in N. brevirostris was oriented anteriorly, with the vertical component accounting for only 34% of the adductive

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185 Table 24. Mechanical advant ages and force distributi ons (N) during feeding in H. francisci N. brevirostris C. plagiosum and H. perlo Variable H. francisci N. brevirostris C. plagiosum H. perlo Opening M.A. 0.89PaP 0.86PaP 0.84PaP n/a Closing M.A. (ant) 0.51PaP 0.34PcP 0.43PbP 0.31PcP Closing M.A. (post) 1.06PabP 1.07PaP 0.83PbP 0.82PbP Opening Force 16PaP 5PbP 12PabP n/a Bite Force (ant) 128PaP 69PbP 69PbP 92PabP (x, y, z) (0, 128, 0) (0, 69, 0) (0, 69, 0) (0, 92, 0) Bite Force (post) 321PaP 217PbcP 127PcP 245PabP (x, y, z) (0, 321, 0) (0, 217, 0) (0, 127, 0) (0, 245, 0) Joint Force (ant) 106PcP 88PcP 59PcP 109PcP (x, y, z) (69, -80*, 0) (87, -10*, 0) (47, -35*, 0) (15, -107*, 0) 49 7 37 82 Joint Force (post) 73PtP 105PtP 47PcP 35PcP (x, y, z) (69, 25, 0) (87, 58, 0) (47, -6*, 0) (15, -31*, 0) 340 326 7 64 Eth. Force (ant) 59PcP 1PtP 51PcP 5PcP (x, y, z) (10, -59*, 0) (-0.9*, 0.3, 0) (18, -46*, 0) (5, -0.4*, 0) 0PP (x, y, z) (0, 0, 0)PP Eth. Force (post) 59PcP 1PtP 51PcP 5PcP (x, y, z) (10, -59*, 0) (-0.9*, 0.3, 0) (18, -46*, 0) (5, -0.4*, 0) 0PP (x, y, z) (0, 0, 0)PP Hyom. Force (ant) 36PtP 2PcP 29PtP 1PtP (x, y, z) (10, 22, 27) (0.9, -0.3, -1) (12, 15, 21) (-0.8*, 0.7, 0.3) 60Pc P (x, y, z) (37, -12, -45)P P Hyom. Force (post) 36PtP 2PcP 29PtP 1PtP (x, y, z) (10, 22, 27) (0.9, -0.3, -1) (12, 15, 21) (-0.8*, 0.7, 0.3) 60Pc P (x, y, z) (37, -12, -45)PP ant, anterior biting; c, compression; Eth, Ethmoidal; Hyom, Hyomandibular; M.A., mechanical advantage; post, pos terior biting; t, tension; angle of the joint reaction force relative to the X-axis Superscript letters denote significant differences fr om statistical analyses P PForces occurring when the ethmoidal ar ticulation disengages during protrusion Negative values indicate forces acting in the negative directi on on their respective axes relative to the right side of the head (see Fig. 30)

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186 Table 25. Resultant jaw adducting forces (N) of H. francisci N. brevirostris, C. plagiosum and H. perlo broken into their principal components Species Resultant Force (N) F x (N) F y (N) F z (N) H. francisci 321 -128* 294 0 N. brevirostris 193 -172* 88 0 C. plagiosum 169 -94* 140 0 H. perlo 308 -30* 306 0 Negative values indicate forces acting in the negative directi on on their respective axes (see Fig. 30) force (Table 25). The vertical component of the adductive force vector is the primary determinant of the bite force th at can be generated for a give n muscular force. Therefore, the vertical orientation of the adductive force vectors in H. perlo, H. francisci and C. plagiosum maximize bite force, whereas the horizont al orientation of the adductive force vector in N. brevirostris will promote the anterior translation of the jaws. Jaw adducting mechanical advantage for biti ng at the anterior margin of the jaws was highest in the durophagous H. francisci followed by C. plagiosum which was greater than both N. brevirostris and H. perlo (F 3,12 = 35.769, p < 0.001). Negaprion brevirostris had higher mechanical advantage ratios for biting at the post erior margin of the functional tooth row than C. plagiosum and H. perlo, all of which were equivalent to H. francisci (F 3,12 = 35.769, p < 0.001) (Table 24). Through the combination of high mechanical advantage ratios and a large, vertically oriented adductive force, H. francisci had the highest anterior (128 N) and posterior (338 N) bite forces. The anterior bite force of H. francisci was significantly grea ter than those of N. brevirostris (69 N) and C. plagiosum (69 N) (F 3,12 = 10.972, p = 0.001), all of which were equivalent to H. perlo (92 N). The posterior bite force of H. francisci was also greater than those of N. brevirostris

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Figure 32. Diagrammatic explanation of local versus global forces acting at articulations within the feeding mechanism, using the jaw joint of N. brevirostris as a model. Arrows within the joint represent equilibrium reaction forces relative to the articular surfaces of skeletal elements (local forces). Arrows acting on skeletal elements represent forces causing kinesis of those skeletal elements (global forces). (217 N) and C. plagiosum (127 N), although the posterior bite force of H. perlo (245 N) was greater than that of C. plagiosum (F 3,12 = 13.044, p < 0.001) (Table 24). The palatoquadrate-mandibular jaw joints of all four species were loaded in compression during anterior biting by virtue of posteroventrally directed local reaction forces relative to the lower jaw (see Fig. 32 for explanation of local versus global reaction forces). Joint reaction forces were highest in H. francisci and H. perlo, which also had the highest anterior bite forces (Table 24). Ratios of joint reaction force to anterior bite force, which are inversely proportional to the relative stability of the fulcrum in a lever system, were highest in N. brevirostris (2.58), followed by H. perlo (2.35), C. plagiosum (1.71), and H. francisci (1.65). Additionally, the large x-axis component of the joint reaction 187

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188 force in N. brevirostris indicates the potential for shearing within its jaw joints. The jaw joints of H. francisci and C. plagiosum experience considerably lower shear forces due to a more equitable balance between the horizon tal and vertical components of the joint reaction forces, while those of H. perlo are loaded nearly in pure compression (Table 24). Compressive loading was identified in the jaw joints of C. plagiosum and H. perlo during posterior biting as well. However, the jaw joints of H. francisci and N. brevirostris exhibited a transition to tensil e loading during posterior biti ng due to their posterior jaw adducting mechanical advantages, both of which exceed 1.0. When the mechanical advantage of a class III lever system exceeds 1.0, the item being bitten is located between the jaw joint and the resultant adductive fo rce vector. At such times the prey item becomes a temporary fulcrum, about which th e adductive muscular forces apply a torque, resulting in tension on the jaw joint (class I le ver system). Ratios of joint reaction force to bite force were again highest in N. brevirostris (1.02), followed by C. plagiosum (0.74), H. francisci (0.43), and H. perlo (0.27). The orientation of the joint reaction force during posterior biting indicates the potential for joint shearing in C. plagiosum as well (Table 24). The ethmoidal articulations of H. francisci C. plagiosum and H. perlo were loaded in compression during both anterior a nd posterior biting due to posteroventrally directed local forces relative to the upper jaw. During biting without upper jaw protrusion, when the ethmoidal articulation of N. brevirostris remains intact, minimal tensile loading occurred (1 N) at this arti culation by virtue of anterodorsally directed local forces relative to the uppe r jaw. When the upper jaw of N. brevirostris is maximally protruded it disengages from the chondrocrani um, precluding loading at the ethmoidal

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189 articulation. The position at which bite force was applied did not change the magnitude or orientation of ethmoidal loading in any of the four species (Table 24). The hyomandibular cartilages of H. francisci C. plagiosum and H. perlo were all loaded in tension to varying extents during anterior and posterior biting. The local forces acting at the hyomandibular articulation relative to the upper jaw were orie nted posterodorsally and medially in H. francisci and C. plagiosum indicating that the hyomandibular cartilages are pulled along thei r longitudinal axes during bitin g (Table 24). Negligible hyomandibular loading (1 N) was oriented anterodor sally and medially in H. perlo. Unlike H. francisci N. brevirostris and C. plagiosum the hyomandibular cartilages of H. perlo are directed anteriorly (Fig. 28). Thus, the orientation of this force places the hyomandibular cartilages of H. perlo in tension as well. Conversely, the hyomandibular cartilages of N. brevirostris were loaded in compression du ring bites both with (62 N) and without (2 N) upper jaw pr otrusion, with much greater lo ading occurring during bites with protrusion. In both s ituations the loca l hyomandibular force was oriented posteroventrally and laterally relative to the jaws, and anterodorsally and medially relative to the hyomandibula (Tab le 24). Hyomandibular loadi ng did not vary with bite position in any of the species. PCA on the mechanics of jaw adduction a nd the resulting force distributions yielded four axes with eigenv ectors greater than 1.0 (93.3% of variance explained). PC1 indicated that the force produ ced by the quadratomandibularis was highly correlated with both anterior and posterior bite force, all of which were correlated with the reaction forces occurring at the jaw joints, ethmoi dal articulation, and hyo mandibular articulation (Fig. 34, Table 26). Hyomandibular force loaded negatively on PC1 indicating a

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Figure 33. Principal components analysis of jaw adducting muscle forces, mechanical advantages, and the resulting force distributions throughout the jaws and their articulations with the cranium in Heterodontus francisci, Chiloscyllium plagiosum, Negaprion brevirostris, and Heptranchias perlo. Variables loading heavily on PC 1 were the force produced by the quadratomandibularis, anterior bite force, posterior bite force, anterior joint reaction force, force at the ethmoidal articulation, and force at the hyomandibular articulation, which loaded negatively. Variables loading heavily on PC 2 were the force produced by the preorbitalis, mechanical advantage for anterior biting, and force at the ethmoidal articulation. Table 26. Results of Principal Components Analysis of jaw adducting and mechanical loading variables in H. francisci, N. brevirostris, C. plagiosum, and H. perlo Variable PC1 PC2 PC3 Preorbitalis Force (N) 0.255 0.782 0.228 Quadratomandibularis Force (N) 0.909 -0.372 -0.143 Anterior Mechanical Adv. 0.398 0.615 0.085 Posterior Mechanical Adv. 0.268 0.055 0.846 Anterior Bite Force (N) 0.957 0.039 -0.049 Posterior Bite Force (N) 0.860 -0.281 0.303 Anterior Joint Reaction Force (N) 0.844 -0.410 -0.016 Posterior Joint Reaction Force (N) 0.214 0.073 0.885 Ethmoidal Force (N) 0.640 0.700 -0.243 Hyomandibular Force (N) -0.549 -0.450 0.45 190

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Figure 34. Regression analyses of reaction forces (N) occurring within the feeding mechanisms of H. francisci, C. plagiosum, N. brevirostris, and H. perlo during prey capture (all species combined). A) Jaw joint reaction force during anterior biting (r 2 = 0.515) and reaction force at the anterior cranio-palatine articulation (ethmoidal or orbital) (r 2 = 0.416) regressed versus anterior bite force. B) Reaction force at the hyomandibular articulation versus anterior bite force (r 2 = 0.525). Positive values indicate compressive loading and negative values indicate tensile loading. C) Absolute value of the reaction forces occurring at the anterior cranio-palatine (r 2 = 0.783) and hyomandibular (r 2 = 0.545) articulations regressed versus the force generated by the preorbitalis muscle. 191

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192 relationship between jaw adducting and bite forces and the magnitude of tensile hyomandibular loading (Figs. 33, 34). The forces generated by the preorbitalis, anterior mechanical advantage, and force at the ethm oidal articulation all loaded heavily on PC2 (Table 26). The preorbitalis is the anterior-most jaw adductin g muscle in all four species, placing it in a position to exert a strong influence over mechani cal advantage. In all four species the preorbitalis inse rts onto the chondrocranium anterior to the ethmoidal articulation as well, giving this muscle hi gh leverage over ethmoidal loading. Posterior mechanical advantage and the joint reaction force for posterior biting loaded heavily on PC3, indicating a correlation be tween the ability of a lever system to transmit force and the resulting reaction forces at th e fulcrum of that lever system. Discussion Prey Capture Biomechanics Differences in the forces produced by th e muscles involved in the expansion of the feeding mechanisms of H. francisci, N. brevirostris and C. plagiosum were did not appear directly related to the use of ram a nd suction feeding by these sharks. Ram feeding involves the predator over-taking its prey and either seizing th e prey between its jaws or engulfing the prey in the buccopharyngeal cavity (Liem, 1980). While rapid jaw adduction is key to capturing elusive prey (Westneat, 1994; Ferry-Graham et al., 2002b; Porter and Motta, 2004), expansion of the feeding mechanism is theoretically less important to ram feeding. Conversely, a quatic suction feeding involves the rapid expansion of the feeding mechanism, which ge nerates a sub-ambient pressure within the buccopharyngeal cavity, causing water and prey to flow into the mouth (Sanford and

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193 Wainwright, 2002; Day et al., 2005). Presumab ly, the rapid production of large forces by the muscles involved in abducting the lo wer jaw and hyobranchial elements would increase the rate of buccopharyngeal expansion (Van Wasse nbergh et al., 2005). However, the abductive muscles of the suction feeding H. francisci and C. plagiosum showed no uniform differences from those of the ram feeding N. brevirostris Although the species means indicated greater force production in the coracomandibularis (lower jaw depressor) and coracoarcua lis (hyoid arch depressor) of H. francisci and C. plagiosum relative to N. brevirostris these differences were only partially supported by statistical analysis (Table 23). While hypertrophication of the primary hyoid (coracohyoideus) and branchial arch (coracobr anchiales) abductors in suction feeding elasmobranchs has been alluded to in nu merous studies (Moss, 1965, 1977; Motta and Wilga, 1999; Motta et al., 2002; Motta, 2004) no support for this assertion was found within these species. Rapid expansion of the feeding mechanism in suction feeding teleosts is generally associate with low (velocity efficient) jaw abducting mechanical advantage ratios (Wainwright and Richard, 1995; Westneat, 1995). However, differences in the ability of H. francisci N. brevirostris, and C. plagiosum to generate suction ca nnot be attributed to the leverage of their jaw abducting mechanis ms either (Table 24). All elasmobranchs exhibit the synapomorphic lower jaw depres sion mechanism of chondrichthyans in which the coracomandibularis inserts onto the poste rior aspect of the mandibular symphysis (Wilga et al., 2000). This developmental constr aint gives all elasmobranchs high leverage (force efficient) jaw abducting mechanisms, especially in comparison to teleosts (M.A. < 0.35) (Wainwright and Richard, 1995; Westn eat, 1995). Based upon the present data, the

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194 question of why suction feedi ng elasmobranchs depress their lower jaws faster than ram feeding elasmobranchs remains unanswered (M otta, 2004; Ch. 4). Varying magnitudes of motor unit recruitment or differential contra ction velocities of th e jaw and hyobranchial abducting musculature, as determined by the myosin isoforms comprising these muscles (Hoh, 2002), may be associated with these performance differences. Additionally, the coracoarcualis and coracomandibularis or co racohyoideus may act as serially-contractilemuscle-units during lower jaw and hyoid ar ch abduction. Both the coracomandibularis and coracohyoideus originate on the antero-v entral surface of the coracoarcualis, such that co-contraction of the coracoarcualis and either of these muscles would increase the force transmitted to the lower jaw and hyoid arch respectively. The coracomandibularis and coracohyoideus are active prior to activation of the coracoarcualis in N. brevirostris and the obligate suction feeding nurse shark Ginglymostoma cirratum (Motta et al., 1997; Matott et al., 2005). If tension has developed in the coracomandibularis or coracohyoideus prior to contraction of the coracoarcu alis, these muscles may act as muscular tendons, transmitting force to the lower jaw or hyoid. The larger forces produced by the coracoarcualis in H. francisci and C. plagiosum may therefore augment the rate at which the lower ja w and hyoid arch are abducted. The mechanics of jaw adduction in H. francisci H. perlo, N. brevirostris and C. plagiosum demonstrated stronger relationships w ith these sharks prey capture and processing methodologies. Heterodontus francisci which consumes hard prey including molluscs and echinoderms (Strong Jr., 1989; Huber et al., 2005), had the highest adductive forces, highest anterior jaw adducti ng mechanical advantage, and highest bite forces of the four species (Tables 23, 24). Its jaw adducting mechanical advantage is

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195 higher than those of all other cartilaginous fishes, with the exception of the durophagous spotted ratfish Hydrolagus colliei (Huber et al., in prep), a nd nearly all actinopterygian fishes with the exception of the durophagous pa rrot fishes (Scaridae) (Turingan et al., 1995; Durie and Turingan, 2001; Huber and Motta, 2004; Wainwright et al., 2004; Westneat, 2004; Huber et al., 2006 ). This high-leverage mechanism is due, in part, to the derived anterior placement and vertical orientation of th e preorbitalis muscle in heterodontiform and orectolobiform sharks (Compagno, 1977). Through the combination of high magnitude, cyclically applied bite forces, robust jaws, and molariform teeth, H. francisci is well suited for crushing the composite exoskeletons of benthic invertebrate prey (Summers et al., 2004; Huber et al., 2005). Although the adductive musculature of H. perlo can generate forces comparable to that of H. francisci its low jaw adducting mechanical advantage ultimately yielded intermediate bite forces. This force-inefficient mechanism is apparently related to constructional constraints asso ciated with the ancestral cr anial morphotype of sharks (Compagno, 1977). The cleaver-shaped upper jaw of extinct cladodont and hybodont sharks, and extant hexanchiform (sixgill, se vengill, frill) sharks, is characterized by a large otic process with a deep fossa in th e quadrate region, posterior to the orbit. The anterior portion of the uppe r jaw is a narrow palatine ra mus that extends beneath the extremely large orbit to approximately the terminus of the head (Fig. 28C) (Allis, 1923; Daniel, 1934; Schaeffer, 1967; Compagno, 1977). The quadrate fossa is paired with a mandibular fossa, both of which are occupied by the large quadratomandibularis muscle. As such, the vast majority of th e jaw adducting musculature (93% in H. perlo) is located posterior to the orbit, resulting in the poor leverage of the jaw adducting mechanism. The

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196 need for large eyes (visual sensitivity) in the light depauperate deep sea environment may be the selective pressure maintaining this anatomical arrangement in H. perlo, which can be found as deep as 1000 m (Compagno, 1984a). Visual constraints on suspensorial anatomy have been identified in cichlid fish es as well (Barel et al., 1989). Given this constraint, the vertical orient ation of the quadratomandibular is maximizes the bite force of H. perlo by producing muscular force nearly orthogonal to the lower jaw. This configuration will help H. perlo grasp and retain elusive pr ey with its fang-like upper teeth, and saw through prey with its multicuspi d lower teeth (Bigelow and Schroeder, 1948; Schaeffer, 1967). Comparing the cranial anatomy of H. perlo to that of N. brevirostris and C. plagiosum demonstrates the general evolutionary pattern of th e shortening and subterminal relocation of shark jaws (Fig. 28) Shortening of the jaws (out-levers of jaw adducting mechanism) has generally been hypot hesized to increase the leverage over jaw adduction and subsequently the bite for ce of sharks, as well as allow for a hydrodynamically efficient subterminal mout h (Schaeffer, 1967). Mechanically, this interpretation of shark jaw evolution i gnores changes to the moment arm of jaw adduction (in-lever) via muscular reorganization. The relativel y low anterior mechanical advantage of N. brevirostris demonstrates concomitant se lection on both muscular and skeletal elements of the feeding mechanism in that the shortening and repositioning of the jaws was met with a reorganization of th e adductor musculature, allowing for a subterminal and velocity efficient feeding mechanis m. Consequently, lower jaw elevation occurs faster in N. brevirostris than in other ram feeding sharks (Tricas and McCosker, 1984; Ferry-Graham, 1997, 1998a; Motta et al., 1997; Wilga and Motta, 1998a, 2000;

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197 Motta and Wilga, 2001) and even the ram feeding snapping turtle Chelydra serpentine (Lauder and Prendergast, 1992). High velocity jaw adduction comes at the cost of bite force however, which was low in N. brevirostris In fact, the voluntary bite force of N. brevirostris (13 N) is significantly lower than the present theoretical estimates of maximum bite force (Ch. 2, 4). Low bite force in N. brevirostris is accommodated for by its sharp, triangular teeth and the routine use of upper jaw protrusion and head shaking to gouge and slice through its prey (Frazzetta and Prange, 1987; Motta et al., 1997). The bite forces of N. brevirostris and C. plagiosum were equivalent despite considerable differences in the mechan isms producing those forces. The adductor musculature of C. plagiosum produced nearly 20% less force than that of N. brevirostris. However, this force was applied to the lower jaw more orthogonally and at a significantly higher mechanical advantage. Despite being cl assified as a suction feeder (Lowry, 2005), the jaw adducting mechanical advantage of C. plagiosum (0.43) was comparable to those of durophagous teleosts considered to be hard prey specialists (Westneat, 2004). The derived anterior placement and vertical orientation of th e preorbitalis muscle in orectolobiform and heterodontiform sharks ac counts for the high mechanical advantage of C. plagiosum (Compagno, 1977). While C. plagiosum consumes a variety of crustacean prey (Compagno, 2001), these quarry do not rival the hardness of the prey of durophagous teleosts and elasmobranchs such as H. francisci (Wainwright et al., 1976; Currey, 1980; Korff and Wainwright, 2004). It is interesting to note that the jaw adducting mechanical advantage of every shark that has been studied, irrespective of their prey capture methodology (ram, suction, b iting), is similar to those of durophagous,

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198 biting teleosts considered to have high le verage jaw adducting mechanisms (M.A. > 0.35) (Huber and Motta, 2004; Westneat 2004; Huber et al., 2005, 2006). Lever systems with high mechanical adva ntage are inherently more stable than low leverage systems because a greater pe rcentage of the muscular force actuating movement is transmitted along the out-lever, leaving a smaller pe rcentage of that force to be balanced by reaction forces within the joint. Accordingly, those species with the highest anterior mechanical advantages ( H. francisci, C. plagiosum ) had the lowest ratios of joint reaction force to bite force for anterior biting. The high ratio of joint reaction force to bite force for anterior biting in H. perlo wont necessarily compromise joint function because the compressive reaction forc e is oriented nearly orthogonal to the articular surface of the joint cartilages, which are strongest in axial compression (Summers and Long Jr., 2006). However, the acute orientation of the reaction force during anterior biting in N. brevirostris will induce shear stre sses at these articular surfaces, and may explain the presence of a large caudal prominence on the lateral quadratomandibular jaw joint in N. brevirostris (Fig. 28). This vertical extension of the joints articular surface may acco mmodate reaction forces occurring over a wide range of gape angles. The extent to which the jaw joints are loaded in axial or shear compression is determined by the orientation of the resultant adductive force vector, which was vertically directed in H. perlo and anteriorly directed in N. brevirostris Compression of the jaw joints duri ng posterior biting occurred in H. perlo and C. plagiosum because their posterior mechanical advantage ratios did not exceed 1.0. Although the joint reaction forces of H. perlo were approximately orthogonal to the articular surface, those of C. plagiosum were acutely oriented. Unlike N. brevirostris the

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199 articular surface of the quadratomandibular jaw joint in C. plagiosum lies completely in the frontal plane, with no caudal prominence to resist shearing within the joint (Fig. 28). Potentially greater joint instabilit y was found during posterior biting in H. francisci and N. brevirostris, in which mechanical advantage ratios greater than 1.0 caused tensile joint loading because the prey becomes a tem porary fulcrum between the jaw joint and resultant adductive force vector. Separation or slippage within the jaw joints due to tensile and shear loading must be prevente d by the complex ligamentous arrays binding the mandibular and hyoid arches together in H. francisci N. brevirostris and C. plagiosum (Daniel, 1915; Motta and Wilga, 1999; Goto, 2001). Jaw Suspension Mechanics Heptranchias perlo retains the amphistylic jaw suspension of its cladodont predecessors, while H. francisci C. plagiosum and N. brevirostris evolved the hyostylic jaw suspension mechanism characteristic of galeomorph neoselachians (Daniel, 1934; Compagno, 1977). Despite having considerably different cranial anatomies, the jaw suspensions of H. perlo, H. francisci and C. plagiosum are functionally analogous in that the anterior cranio-palatine articulation (ethmo idal or orbital) remains intact during the full range of motion exhibited by the jaws (Compagno, 1977; Maisey, 1980; Motta et al., 1997; Huber et al., 2005). Subsequently, th e common suspensorial loading pattern observed in these sharks invol ved compression at the anterior cranio-palatine articulation (ethmoidal or orbital) and tension at the posterior hyoma ndibular articulation. Conversely, the jaw suspension of N. brevirostris experienced negligible tension at its ethmoidal articulation and compression at th e hyomandibular arti culation during bites without protrusion, and substantial hyomandibular compression during bites with

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200 protrusion. Negaprion brevirostris is capable of protruding the upper jaw far enough that it loses contact with the ethmoid region of the cranium (Motta and Wilga, 1995). The common denominators underlying these differences in suspensorial lo ading are the state of the anterior cranio-palatin e articulation (intact or disart iculated), and the presence or absence of a force vector acting between the jaws and cranium (pre orbitalis or levator palatoquadrati muscles). The preorbitalis muscles of H. francisci and C. plagiosum originate on the anterior portion of the lower jaw and insert on the cranium posterior to the nasal capsule, while that of H. perlo originates more posteriorly on the median raphe of the quadratomandibularis muscle and inserts on th e cranium posterior to the nasal capsule. As such, the forces produced by the preorbit alis are included in the static equilibrium calculations of the lower jaw, and not the upper jaw. Taking all other muscular and reaction forces to be equal, the inequality of the forces acting on the lower and upper jaws due to the preorbitalis results in the ne t upward translation of the mandibular arch. The nature of this upward translation is dictat ed by the presence or absence of contact at the anterior cranio-palatine articulation (eth moidal or orbital) and the position of the preorbitalis insertion relativ e to this articulation. In H. perlo, H. francisci and C. plagiosum the preorbitalis inserts an terior to the articulation. The resulting moment arm of the preorbitalis compresses the upper jaw into the articul ation and generates a counterclockwise torque about this poi nt relative to the right side of the head (Fig. 35). As a result, the posterior region of the upper jaw rotates anteroventrally, pulling the hyomandibular cartilages in tension (Fig. 35, Table 27). This loading regime was

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Figure 35. Right lateral views of the feeding mechanisms of (A) C. plagiosum and (B) N. brevirostris indicating the net forces acting on the jaws and their articulations with the cranium during biting. Black arrows with C indicate compressive loading, black arrows with T indicate tensile loading, and white arrows with black outlining indicate the direction of motion of the jaws due to the net muscular force acting on the feeding mechanism. (A) During biting in C. plagiosum (representative of H. francisci and H. perlo) the ethmoidal articulation remains intact. As the jaws translate upwards via muscular force acting between the jaws and cranium, they compress and pivot about the ethmoidal articulation. The resultant rotation of the jaws pulls the hyomandibular cartilages in tension. (B) During biting at maximum protrusion in N. brevirostris the upper jaw disarticulates from the cranium at the ethmoidal articulation. Unable to pivot about the ethmoidal articulation, upward translation of the jaws occurs in a linear manner, compressing the hyomandibular cartilages against the cranium. supported by the PCA, which indicated strong correlations between the force generated by the preorbitalis, the magnitude of compression at the anterior cranio-palatine articulation, and the magnitude of tension at the hyomandibular articulation (Fig. 34, Table 26). The primary muscles actuating upper jaw protrusion in N. brevirostris are the ventral division of the preorbitalis and levator palatoquadrati, each of which generate force between the jaws and cranium (Motta and Wilga, 1995; Motta et al., 1997). Biting without protrusion was modeled assuming inactivity in these muscles, and the resulting 201

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equilibrium conditions lacked a force vector between the jaws and cranium. Despite the fact that the anterior cranio-palatine articulation remains intact during bites without 202 protrusion, the resultant suspensorial loading showed negligible tension at this articulation (1 1 N) and negligible compression on the hyomandibular cartilages (2 1 N). Taking the respective standard error estimates into account, the suspensorium of N. brevirostris effectively experiences no loading during bites without protrusion because all muscular and reaction forces are equally applied to both the lower and upper jaws (no net translation of the jaws). During protrusion in N. brevirostris, disengagement of the upper jaw from the cranium precludes the generation of torque about the anterior cranio-palatine articulation.

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203 With no erior to rbitalis (D.R. drati per the anterior craniopalatine rlo ; e of pivot point, activity in the ventral pr eorbitalis and levator palatoquadrati causes a net upward translation of the mandibular arch resulting in compression on the hyomandibulae (60 N), which are located between the jaws and cranium (Fig. 35, Table 27). If these muscles were active prior to protrusion and dissociat ion of the ant cranio-palatine articulation, a torque about the articulation would still favor hyomandibular compression because the levato r palatoquadrati inserts posterodorsal the articulation and generates a larger bending moment than the ventral preo Huber, unpub. data). This scenario is specific to carcharhinid sharks, the only group in which the levator palatoquadrati is oriented anterodorsally allowing it to participate in upper jaw protrusion (Compagno, 1988; Wilga et al., 2001). Regardless, the motor activity pattern duri ng jaw adduction in N. brevirostris suggests that activity of the quadratomandibularis pulls the upper jaw vent rally, disengaging the anterior craniopalatine articulation, prior to activity in the ventral preorbit alis and levator palatoqua (Motta et al., 1997). In other elasmobranchs the levator palatoquadr ati retracts the up jaw during the recovery phase of the gape cycle (Wilga, 2005). Presuming that suspensorial loading is determined by the position of muscular force vectors acting between the jaws and cranium and whether articulation is intact or dissociated, the nature of suspensorial loading can be hypothesized in other groups of elasmobranchs (Table 27). The configuration of the preorbitalis in orbitostylic squalean sharks such as S. acanthias is the same as in H. pe the preorbitalis is a single headed, horizontal muscle extending from the median raph the quadratomandibularis muscle to the posteri or aspect of the nasal capsule (Wilga and Motta, 1998a). The orbital process of the uppe r jaw maintains contac t with the cranium

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204 the goblin s derived at r jaw is e throughout the full range of motion exhibi ted by the jaws as well (Compagno, 1977; Wilga and Motta, 1998a). Theref ore it is hypothesized that S. acanthias and other orbitostylic sharks in which the orbital articulation remains intact during feeding will exhibit compression at the orbital articu lation and tension on the hyomandibulae. Wilga (2005) recently identified additiona l variants of the traditional hyostylic jaw suspension in lamniform sharks. The jaw suspension of basal lamnoids such as Mitsukurina owstoni sandtiger Carcharias taurus, and common thresher sharks Alopias vulpinnis is characterized by suspenso ry hyomandibular cartilages and ligamentous connections between the upper ja w and both the ethmoidal and nasal region of the cranium. Derived lamnoids such as the porbeagle Lamna nasus white Carcharodon carcharias and shortfin mako sharks Isurus oxyrinchus have suspensory hyomandibulae and have lost the ethmopalatin e ligaments while retaining the palatonasal ligament. All of these sharks are capable of extensive jaw protrusion such th the upper jaw can disarticulate from the cr anium (Tricas and McCosker, 1984; Wilga, 2005). Mitsukurina owstoni and A. vulpinnis are have preorbitalis muscles extending from the jaws to the cranium, while the preorbitalis of C. carcharias C. taurus, I. oxyrinchus, and L. nasus lie between the lower and uppe r jaws (Wilga, 2005). Like N. brevirostris during bites with protrusi on, activity of the preorbita lis while the uppe dissociated from the cranium in M. owstoni and A. vulpinnis will hypothetically place th hyomandibular cartilages in compression. The lack of a preorbitalis force vector between the jaws and cranium in C. carcharias C. taurus I. oxyrinchus and L. nasus apparently indicates negligible suspensorial loading in these sharks. However, the novel insertion of the levator hyomandibularis muscle onto th e upper jaw in derived lamnid sharks ( I.

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205 ape (euhyostyly) (Wilga role in n. rce sm es oxyrinchus, L. nasus C. carcharias ) is suggestive of hyomand ibular compression as well (Table 27). From this insertion point, th e levator hyomandibularis can direct precise movements of the upper jaw by bracing it ag ainst the cranium via the hyomandibular cartilages, perhaps allowing for repeated protrusion of the upper jaw during a single g cycle (Tricas and McCosker, 1984; Wilga, 2005). Additionally, all lamniform sharks possess a sesamoid-like cartilage in their novel palatonasal ligame nts, suggestive of tensile forces at the anterior cranio-palatine articulation (Wilga, 2005). The batoids lack an anterior cran io-palatine articulation, making the hyomandibular cartilages the sole support of the jaws against th e cranium 2002). The quadratomandibularis and pr eorbitalis play a synergistic protruding the jaws anteroventrally, with th e preorbitalis exerting force between the lower jaw and the cranium (Wilga and Mo tta, 1998b). This mechanism is again analogous to the suspensorial mechanics of N. brevirostris during bites with protrusio The lack of anterior cranio-palatine contact coupled with an upwardly directed fo between the jaws and cranium will hypotheti cally result in hyomandibular compression (Table 27). Additionally, batoids possess several novel lower jaw and hyomandibular depressor muscles that appear to pivot (com press) the jaws and hyomandibulae about the cranium allowing for high-precision, asymmetr ical movements of the feeding mechani (Miyake et al., 1992; Wilga and Motta, 1998b; Dean and Motta, 2004a; Dean et al., 2005b). Although a modeling analysis has not be en performed on a batoid, trabecular reinforcement in the jaws a nd hyomandibular cartilages of N. brasiliensis corroborat the role of the hyomandibulae as compressive elements. Medial translation of the hyomandibular cartilages protrudes the jaws of N. brasiliensis such that at maximum

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206 s. e H. perlo are suggestive of a broad evolutionary pattern in elasmobranch feeding mechan he r lar ylic ig. 29) (Schaeffer, 1967; Carroll, 1988). Due to the abutme o protrusion the longitudinal axes of the hyom andibulae line up with those of the jaw Trabeculae in the jaws and hyomandibular carti lages are arranged to resist buckling as the jaws are axially buttressed against th e cranium during protrusion (Dean and Motta 2004a, 2004b; Dean et al., 2005a). Collectively, enhanced maneuverability of the jaws appears to be associated with hyomandibular compression in elasmobranchs in which th anterior cranio-palatine articulation is e ither permanently or temporarily disengaged. Evolution of Jaw Suspension The suspensorial mechanics of H. francisci C. plagiosum N. brevirostris and isms. The available evidence indicate s that the amphistylic jaw suspension was characterized by negligible suspensorial lo ading because the vast majority of t adductive force acted betw een the jaws (93% in H. perlo), not between the jaws and cranium. Under these conditions there would have been litt le selective pressure fo structural changes to the long, thin, poorly calcified, posteri orly directed hyomandibu cartilages of extinct (cladodont, early hybodont) and extant (hexanchiform) amphist sharks (Zangerl and Williams, 1975; Maisey, 1980). Thus, the hyoid arch retained the appearance of the post-mandibular visceral ar ch from which it was derived (Zangerl and Williams, 1975; Mallatt, 1996). An obvious characteristic of the cranium in these sharks are the large, laterally expanded postorbital processe s (F nt of the otic process of the upper jaw against this protuberance, it would have impeded anterior and perhaps even ventral tran slation of the jaws. Therefore, there als would have been little selective pressure for the preorbitalis to diversify in these sharks

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207 ard, avity or de of aeffer, 1967; Maisey e of Provided that the postorbital articulation did not prevent ventral translation of the upper jaw, protrusion would have occurred in th e vertical plane when the lower jaw was depressed and contraction of the quadratoma ndibularis adducted th e upper jaw towards the lower jaw. Contraction of the preorbit alis would have drawn the upper jaw forw compressing it into the postorbi tal articulation and generating a small counter-clockwise torque about this articulation relative to the right side of th e head, analogous to compression at the orbital articulation in H. perlo. This mechanism would have braced the upper jaw against the cran ium and possibly expanded th e buccopharyngeal c assisted in retracting the protruded upper jaw (Schaeffer, 1967). Therefore, the plesiomorphic suspensorial loading regime associated with the amphistylic jaw suspension probably involved compression be tween the upper jaw and cranium at the postorbital articulation and tension on the hyomandibular cartilages, the magnitu which was dictated by the force of the preorbitalis (Fig. 34, Table 27). Once the postorbital articulation was conve rgently lost via reduction of the otic process of the upper jaw in the late hybodontoids and neoselachians (Sch 1982; Carroll, 1988; Ma isey and de Carvalho, 1997), architectural changes to th preorbitalis (enlargement, s ubdivision, reorientation) woul d have facilitated anterior movement of the jaws, in addition to the existing ventral motion. Anterior kinesis would have been further facilitated by the reduction of the postorbital process on the cranium neoselachians as well (Schaeffer, 1967; Carroll, 1988). As this modeling analysis indicates, increased force pr oduction by the preorbitalis caus es increased loading at the anterior cranio-palatine and hyomandibular ar ticulations, providing the impetus for the evolution of the hyostylic jaw suspension m echanism. Subsequently, the hyomandibular

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208 ; Fig. e e evolution of hyostyly appears to have been cap italized upon by carcharhinid, lamnoi ilga cartilages of the neoselachians became shorter, thicker, rotated anteriorly into a more orthogonal position relative to the cranium, a nd developed deep articular facets against the cranium facilitating dire ctionally specific motion (Schaeffer, 1967; Cappetta, 1987 Wilga, 2002). These characteristics are indi cative of the hyomandibular cartilages being drawn forward under a repeatable loading regime and suggest that these elements play a passive role in bracing the jaws during protrusion. The hyom andibular cartilages of the late hybodontoids also increased in size conc omitant with the loss of the postorbital articulation. However, these hyomandibulae were located dorsal to the upper jaw and remained posteriorly directed, suggesting that they were less suited for load-bearing ( 28) (Maisey, 1980, 1982, 1987). Additionally, the uppe r jaws of these sharks abutted th postorbital region of the cranium, making them functionally amphistylic (Schaeffer, 1967). The general increase in load-bearing ability of the hyomandibular cartilages during th d, and batoid elasmobranchs. In each of these groups, dive rsification of the muscles controlling jaw and hyomandibular movement has led to increased magnitude and precision of jaw kinesis (Moss, 1977; Compagno, 1988; Miyake et al., 1992; W and Motta, 1998b; Wilga et al., 2001; Dean and Motta, 2004b; Wilga, 2005). Enhanced jaw kinesis is associated with the dissocia tion of the upper jaw from the cranium and a subsequent transition from te nsile to compressive hyomandi bular loading, allowing the jaws and hyomandibulae to be pivoted about the cranium. This pivoting is believed to permit repeated protrusion during a singl e gape cycle in lamniform sharks and asymmetric strikes at prey in batoids (D ean and Motta, 2004b; Wilga, 2005). Therefore

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209 alatine roperties echanical principles elucidated by this study allow inferences to be drawn regarding of fish through evoluti to d in the hyomandibular compression probably preceded th e loss of the anterior cranio-p articulation during the evolu tion of euhyostyly in batoid s. Because the nature of hyomandibular loading is determined by the ty pe of jaw suspension and the extent of muscular control over jaw protrusion, hyo mandibular morphology and material p (as indicative of load-bearing ability) may vary concomitantly with these parameters in elasmobranchs. Jaw Suspension Mechanics in Non-Elasmobranch Fishes The biom the jaw suspension mechanisms of other major radiations onary history. The extinct placoderms are believed to be either the sister-group chondrichthyans (Janvier, 1996; Liem et al., 200 1) or the sister-group to all gnathostomes (Goujet, 2001). Most placoderms had a rudime ntary holostylic jaw suspension in which the quadrate portion of the upper jaw was fu sed to the robust dermal skeleton (MoyThomas and Miles, 1971; Carroll, 1988). Am ong fishes, only the hol ocephalans (sistertaxon to the elasmobranchs) have a truly holostylic jaw suspension characterized by complete fusion of the upper jaw to the cr anium and a non-suspenso ry, intact hyoid arch (Grogan et al., 1999). This mechanism is distin ct from the autostylic mechanism foun sarcopterygian fishes and tetrapods, in whic h the upper jaw is fused to the cranium and hyoid arch is non-suspensory and broken-up or modified (Liem et al., 2001; Wilga, 2002). Although the hyomandibula was located between the jaws and cranium in placoderms, the upper jaw was akinetic in mo st taxa and could not induce loading on hyomandibula (Moy-Thomas and Miles, 1971 ). The only load-bearing activity the hyomandibula may have performed in these fish es was during cranial elevation via their

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210 cted s. These fish possessed an orbital cranio-palatine articulation and long, thin hy iles, fore, it cannot e ison, 1979; L al ontribution novel cranio-thoracic joint in the dermal armor because the dermal armor was conne to the upper jaw, which was in turn conn ected to the hyomandi bula (Moy-Thomas and Miles, 1971). The derived rhenanid placoderms were the only group known to possess protrusible jaw omandibular cartilages that were cl early suspensory (Moy-Thomas and M 1971; Carroll, 1988). Protrusion would have occu rred in the vertical plane as the upper and lower jaws were adducted towards each other via contraction of the quadratomandibularis. However, the presence or absence of an additional muscle acting between the jaws and cranium such as the pr eorbitalis is unknown. There be determined whether the hyomandibular car tilages of rhenanid placoderms were actually load-bearing. The genera l lack of calcification in th ese cartilages suggests that they were not load-bearing (Moy-Thomas and M iles, 1971; Wilga, 2002). The acanthodians, sister-group to the os teichthyan fishes, also had hyomandibula articulating with the upper jaw and craniu m (Moy-Thomas and Miles, 1971; Den iem et al., 2001). As with the placoderms, the existenc e of cranio-palatine muscle forces in these fish is unknown and the nature of hyomandibular loading cannot be determined. Hyomandibular loading is believed to have been negligible if present at all, because the upper jaw had prominent articulat ions with both the basal and postorbit regions of the cranium. Therefore, the hyomandibulae of acanthodians are believed to have been non-suspensory (Moy-Th omas and Miles, 1971; Denison, 1979). The lower jaw of the osteichthyan fishes is braced against the cranium via the suspensorial series of bones, with the quadr ate forming the suspensoriums c

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211 to the l f talized ous ing it ower jaw joint distally and the hyo mandibula articulating with the neurocranium proximally. As such, the hyomandibula is directly in series with the jaw joint. The lower jaw adducting mechanism of the osteichthyans is a class III lever system with the bulk o the adductor musculature originating on and ar ound the suspensorium and inserting onto the lower jaw (Winterbottom, 1974). Given this musculoskeletal geometry, the jaw joint will be loaded in compression during biting provided that bite force is applied anterior to the resultant adductive force vector. This compressive joint re action force will be transmitted up the suspensorium, compressing the hyomandibula into the cranium. Independence of the upper jaw from the lowe r jaw adducting mechanism was capi upon by the actinopterygian radiation of oste ichthyan fishes, which developed numer mechanisms of protruding the upper jaw (S chaeffer and Rosen, 1961; Alexander, 1967; Motta, 1984). Protrusibility of the upper jaw is considered a key innovation in the adaptive radiation of modern actinopterygian fishes, as it permitted the diversification of a myriad of feeding specializations (S chaeffer and Rosen, 1961). The evolutionary progression towards enhanced cranial kinesis in these fishes has been associated with the shortening, thickening, and more orthogonal orientation of the hyomandibulae, all suggestive of an increase in load-beari ng activity (Schaeffer and Rosen, 1961). Some modern actinopterygian fishes have evolved kinesis within the suspensorium, allow to pivot independently of the skull and pr otrude the lower jaw as well (Westneat and Wainwright, 1989; Ferry-G raham et al., 2001b).

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212 Conclusions In the absence of load-bearing activity sk eletal elements lack the mechanical impetus needed to adaptively diversify is believed to be the cranial archetype for elas due tion anical of the elasmobranch feeding mechanism increased dramat in way ss with Given wh at mobranchs, the amphistylic jaw su spension mechanism was not load-bearing to small forces produced by the muscles acting between the jaws and cranium. As a result, the hyoid arch retained the structure of a post-mandibular visc eral arch. Given this mechanical context for skeletal diversificati on, the most likely scenario for the evolu of hyostyly from amphistyly involved a ugmentation of the force produced by the preorbitalis and concomitant loss of the postorbital articulation, followed by hyomandibular diversification. Once the hyomandibula was better able to receive and distribute mech loading, the evolutionary lability ically. Enhanced jaw kinesis likely in creased the effectiveness of ram feeding elasmobranchs by providing quicker gape closure and the ability to extend the jaws a from the head to excise large chunks of pre y. By freeing the posterior margin of the jaws from the cranium, hyostyly permitted shortening and subterminal placement of the jaws. Barring reorganization of the adductor musculat ure, shortening of the jaws increased the leverage of the feeding mechanism and the ab ility of benthic elasmobranchs to consume hard prey. Lastly, increase d load-bearing abili ty of the hyomandibula would have allowed for forceful, rapid movements of the hyoid arch as re quired during suction feeding. Collectively, these change s illustrate that kinesis increased the effectivene which the jaws could be used as tools for prey capture, and that elasmobranchs capitalized upon this by radically diversifying the feeding mechanism in modern forms.

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231 Appendices

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232 Appendix I: Mass-Specific B ite Forces of Vertebrates Vertebrate Group Source Specific Name Common Name Ante rior Bite Force (N) Mass (g) Residual Bite Force Mammals Ringqvist (1972) Homo sapiens human 294 55000 -1.21 Robins (1977) Rattus norvegicus Norway rat 47 555 0.06 Thomason et al. (1990) Didelphis virgin iana North American opposum 442 5000 1.13 Binder and Van Valkenburg (2000)* Crocuta crocuta spotted hyena 242 20700 -0.74 Crocuta crocuta spotted hyena 2195 292000 0.05 Thompson et al. (2003) Monodelphis domestica short-tailed opposum 21 90 0.32 Wroe et al. (2005) Acinonyx jubatus cheetah 472 29500 -0.15 Alopex lagopus Arctic fox 178 8200 -0.40 Canisalpinus dhole 314 16500 -0.21 Canis aureus golden jackal 165 7700 -0.45 Canislatrans coyote 275 19800 -0.53 Canis lupus dingo dingo 313 17500 -0.25 Canis lupus hallstromi singing dog 235 12300 -0.36 Canis lupus lupus grey wolf 593 34700 0.01 Dasyurus maculatus spotted-tailedquoll 153 3000 0.15 Dasyurus viverrinus Eastern Quoll 65 870 0.02 Felisconcolor cougar 472 34500 -0.28 Felis sylvestris wild cat 56 2800 -1.04 Felis yagouaroundi jaguarundi 127 7100 -0.73 Gennetta tigrinum striped genet 73 6200 -1.32 Hyaena hyaena brown hyena 545 40800 -0.20 Lycaon pictus African hunting dog 428 18900 0.06 Lynxrufus bobcat 98 2900 -0.37 Melesmeles Europeanbadger 244 11400 -0.25 Neofelisnebulosa clouded leopard 595 34400 0.01 Pantheraleo lion 1768 294600 -0.22 Pantheraonca jaguar 1014 83200 0.05 Pantherapardus leopard 467 43100 -0.43 Pantheratigris tiger 1525 186900 -0.07 Protelescristatus aardwolf 151 9300 -0.70 Sarcophilus harrisii Tasmanian devil 418 12000 0.38 Thylacinus cynocephalus Tasmanianwolf 808 41700 0.28

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233 Appendix I (Continued) Ursus americanus black bear 751 128800 -0.67 Ursus americanus black bear 751 128800 -0.67 Ursus arctos brown bear 312 77200 -1.42 Ursus thibetanus Asiatic bear 244 11400 -0.25 Vulpes vulpes red fox 164 8100 -0.51 Reptiles Cleuren et al. (1995) Caiman crocodilus spectacledcaiman 70 1500 -0.28 Herrel et al. (1999) Gallotia ga lloti Canary Islandlizard 109 58 2.73 Herrel et al. (2001) Xenosaurus grandis knob-scaled lizard 12 17 1.09 Xenosaurus newmanorum crevice-dwelling lizard 19 27 1.27 Xenosaurus platyceps crocodile lizard 20 25 0.91 Herrel et al. (2002) Amyda cartilagi nea Asian softshell turtle 210 937 1.44 Apalone ferox Florida softshell turtle 42 114 0.99 Apalone spinifera spiny softshell turtle 12 260 -1.17 Callagur borneoensis pa inted terrapin 147 10065 -0.79 Chelus fimbriatus matamata 5 405 -2.62 Chelydra serpentina snapping turtle 209 3940 0.35 Chinemys reevesii Reeve's turtle 20 137 -0.07 Dogania subplana Malayan softshell turtle 37 328 0.05 Elseya novaeguineae New Guinea snapping turtle 35 743 -0.64 Emydura subglobosa red-bellied short-necked turtle 2 119 -2.86 Geoemyda spengleri black breasted leaf turtle 12 126 -0.64 Heosemys grandis giant Asian pond turtle 102 2866 -0.31 Kinosternon scorpioides sc orpion mud turtle 38 214 0.41 Kinosternon subrubrum Mississippi mud Turtle 35 133 0.66 Macrochelys temminckii alligator snapping tu rtle 158 388 1.75 Orlitia borneensis Malaysia n giant turtle 117 3818 -0.34 Pelodiscus sinensis Chinese softshell turtle 59 305 0.70 Pelomedusa subrufa African helmeted turtle 8 224 -1.59 Phrynops nasutus common toad-headed turtle 432 1752 1.89 Platemys platycephala twist-necked turtle 7 245 -1.80 Platysternon megacephalum big-headedturtle 42 137 0.86 Staurotypus salvinii Pacific coast giant musk turtle 252 743 1.84 Staurotypus triporcatus Mexican giant musk turtle 139 600 1.25

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234 Appendix I (Continued) Sternotherus carinatus razorback musk turtle 109 276 1.55 Sternotherus odoratus common musk turtle 31 321 -0.16 Terrapene carolina box turtle 25 361 -0.51 Testudo horsfieldii Russian tortoise 18 373 -0.93 Trachemys scripta common slider turtle 15 235 -0.82 Erickson et al. (2004)* A lligator mississippiensis American alligator 217 1650 1.06 Alligator mississippiensis American alligator 13172 242700 2.48 Birds Van der Meijj and Bout (2004) Amadina er ythrocephala red-head ed finch 4 23 -0.74 Amadina fasciata cut-throat finch 5 19 -0.24 Carduelis chloris European greenfinch 14 28 0.64 Carduelis flammea common redpoll 3 13 -0.70 Carduelis sinica grey-capped greenfinch 8 20 0.26 Carduelis spinus Eurasian siskin 3 13 -0.63 Carpodacus erythrinus common rosefinch 6 22 -0.11 Chloebia gouldia Gouldian finch 4 15 -0.40 Eophona migratoria yellow-billed grosbeak 36 52 1.41 Erythrura trichroa blue-faced parrotfinch 5 13 0.02 Estrilda troglodytes black-rumped waxbill 1 7 -1.52 Hypargos niveoguttatus Peters twinspot 3 16 -0.80 Lagonostictasenegala redbilled firefinch 1 7 -1.35 Lonchura fringilloides magpie munia 5 16 -0.19 Lonchurapallida pale-headedmunia 3 13 -0.56 Lonchura punctulata scaly-breasted munia 4 12 -0.36 Mycerobas affinis collared grosbeak 38 70 1.24 Neochimamodesta plum-headedfinch 2 13 -1.20 Neochima ruficauda star finch 2 12 -1.07 Padda oryzivora java sparrow 10 30 0.15 Phoephila acuticauda l ong-tailed finch 3 8 -0.53 Poephilacincta black -throated finch 3 16 -1.04 Pyrrhula pyrrhula Eurasian bullfinch 5 21 -0.41 Pytilia hypogrammica red-faced pytilia 3 15 -0.75 Rhodopechys obsoleta desert finch 6 23 -0.12 Serinus leucopygius white-rumped seedeater 2 10 -0.89

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235 Appendix I (Continued) Serinus mozambicus yellow-frontedcanary 3 12 -0.66 Serinus sulphuratus brimstone canary 12 18 0.80 Taeniopygia bichenovi double-barred finch 2 10 -1.03 Taenopygia guttata zebra finch 4 23 -0.77 Uraeginthus bengalus red-cheeked cordonblue 1 10 -1.54 Fish Hernandez and Motta (1997) Archosargus probatocephalus sheepshead 309 998 1.88 Clifton and Motta (1998) Halichoeres bivittatus slipperydick 5 19 -0.35 Halichoeres garnoti yellowhead wrasse 10 21 0.49 Halichoeres maculipinna clown wrasse 11 18 0.71 Lachnolaimusmaximus hogfish 290 209 2.97 Thalassoma bifasciatum bluehead wrasse 5 7 0.47 Huber and Motta (2004) Squalus acanthias spinydogfish 20 501 -1.09 Huber et al. (in prep) Hydrolagus colliei white-spotted ratfish 87 870 0.96 Huber et al. (2005) Heterodontus francisci horn shark 206 2948 0.54 Korff and Wainwright (2004) Chilomycterus schoepfi striped burrfish 380 180 3.42 Huber et al. (2006)* Carcharhinus limbatus blacktipshark 32 1274 -0.04 Carcharhinus limbatus blacktip shark 423 22092 -1.15 *Two values are given for studies in which specimen body masses ranged over more than one order of magnitude

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About the Author Born in West Hempstead, NY on December 7, 1978, Daniel Huber spent much of his childhood in and around the Atlantic O cean. At age eight a relative of Dans was bitten by a shark, beginning his lifelong fasc ination with these amazing animals. After graduating from Chaminade High School in 1996, Dan attended Duke University and received his B.S. in Biology in 2000. Dan then began his doctorate at the University of South Florida as an inaugural recipient of the universitys Presidential Fellowship, where he worked under Dr. Philip Motta on the biomechanics and functional morphology of shark feeding. He has taught courses in Co mparative Vertebrate Anatomy and Human Anatomy and Physiology, and has appeared in numerous Discovery Channel productions. At the completion of his doctorate, Dan had authored six papers and in the fall of 2006 will be joining the faculty in the Biology Department at the University of Tampa.