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Evolution of the hammerhead cephalofoil :

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Title:
Evolution of the hammerhead cephalofoil : shape change, space utilization, and feeding biomechanics in hammerhead sharks (sphyrnidae)
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Mara, Kyle
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University of South Florida
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Subjects / Keywords:
Bite force
Performance
Functional morphology
Morphometrics
Constraints
Dissertations, Academic -- Biology-Integrative -- Masters -- USF   ( lcsh )
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non-fiction   ( marcgt )

Notes

Abstract:
ABSTRACT: The relationship between form and function is often used to elucidate the biological role of a structure. Hammerhead sharks offer a unique opportunity to study form and function through phylogeny. Because sphyrnid sharks display a range of cranial morphologies this group can be used to address questions about the evolution of cranial design and investigate the effects of changes in head morphology on feeding structures and bite force. Geometric morphometrics, volumetric analyses, morphological dissections, and phylogenetic analyses of the cephalofoil were used to gain insight into changes in cranial design through evolutionary history. External morphometrics and internal volumetric analyses indicated that while the external shape of the cephalofoil and placement of the sensory structures is variable through evolutionary history, the volumes of the internal cranial elements do not change. Constructional constraints within the cephalofoil were confined to sensory structures while feeding morphology remained relatively unchanged. Analysis of the morphology and biomechanics of the feeding apparatus revealed that through phylogeny the feeding system does not change among sphyrnid species. However, size-removed bite force was lower than predicted for all sphyrnid species except Sphyrna mokarran. Despite differences in head morphology between sphyrnid and carcharhinid sharks, the feeding bauplan is conserved in sphyrnid sharks with few changes to the feeding structures. Instead the chondrocranial and sensory structures are modified around the relatively static feeding core. Finally, the durophagous S. tiburo was found to consume hard prey in a manner that is biomechanically and morphologically different from other durophagous fishes. Furthermore, the diet of S. tiburo is constrained by the properties of its preferred prey.
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Dissertation (PHD)--University of South Florida, 2010.
Bibliography:
Includes bibliographical references.
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by Kyle Mara.
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ABSTRACT: The relationship between form and function is often used to elucidate the biological role of a structure. Hammerhead sharks offer a unique opportunity to study form and function through phylogeny. Because sphyrnid sharks display a range of cranial morphologies this group can be used to address questions about the evolution of cranial design and investigate the effects of changes in head morphology on feeding structures and bite force. Geometric morphometrics, volumetric analyses, morphological dissections, and phylogenetic analyses of the cephalofoil were used to gain insight into changes in cranial design through evolutionary history. External morphometrics and internal volumetric analyses indicated that while the external shape of the cephalofoil and placement of the sensory structures is variable through evolutionary history, the volumes of the internal cranial elements do not change. Constructional constraints within the cephalofoil were confined to sensory structures while feeding morphology remained relatively unchanged. Analysis of the morphology and biomechanics of the feeding apparatus revealed that through phylogeny the feeding system does not change among sphyrnid species. However, size-removed bite force was lower than predicted for all sphyrnid species except Sphyrna mokarran. Despite differences in head morphology between sphyrnid and carcharhinid sharks, the feeding bauplan is conserved in sphyrnid sharks with few changes to the feeding structures. Instead the chondrocranial and sensory structures are modified around the relatively static feeding core. Finally, the durophagous S. tiburo was found to consume hard prey in a manner that is biomechanically and morphologically different from other durophagous fishes. Furthermore, the diet of S. tiburo is constrained by the properties of its preferred prey.
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Evolution of the Hammerhead Cephalofoil: Shape Change, Space Utilization, and Feeding Biomechanics in Hammerhead Sharks (Sphyrnidae) by Kyle Reid Mara A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Integrative Biology College of Arts and Science University of South Florida Major Professor: Philip J. Motta, Ph.D. Stephen Deban, Ph.D. James Garey, Ph.D. Stephen Kajiura, Ph.D. Robert Hueter, Ph.D. Date of Approval: June 28, 2010 Keywords: bite force, performance, func tional morphology, morphome trics, constraints Copyright 2010, Kyle Reid Mara

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DEDICATION I dedicate this work to my parents Richar d and Barbara Mara Jr. They have always supported me in all that I do and without them I could not have accomplished this feat.

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ACKNOWLEDGEMENTS I have been striving toward this goal for the bett er part of my adult li fe. Because of this I cannot possibly list all of the people that have helped me along the way. However, I will try. First I would like to thank my major a dvisor Dr. Philip J. Motta. He has provided valuable assistance, training, and mentorship along the way. He also has also always encouraged me to think outside of the “h ammerhead box.” The number of people that have assisted me in one way or another is truly staggering and I am indebted to their tireless assistance and willingness to go home smelling like shark for me. First and foremost Janne Pfeiffenberger served as my undergraduate assistant for two years, without his help with dissecti ons and laboratory work I coul d not have accomplished this task. Secondly, Erin Faltin has been with me through the best of times and the worst of times during this process and has helped me stay on track when I strayed and provided much needed breaks when necessary. Many ot hers have contributed to this work in various ways including: Drs. Stephen Deba n, Stephen Kajiura, Robert Hueter, James Garey, Andrew Martin, and Florence Thomas. Courtney Phillips, Jessica Davis, Maria Laura Habeggar, Tanya Brunner, Cynthia Fox, Tricia Meredith, Amber Shephard, and Eric Lambert all provided experimental assist ance in various areas of this project. Specimens were generously collected a nd provided by: Sterling Peverell, Daniel Kimberley, Tom, Trnski, Clinton Duffy, Gray ’s Taxidermy, Jose Castro, Frank Snelson Jr., Andrew Piercy, Jack Morr is, the staff of Mote Marine Laboratory, many Trinidadian fisherman, and the Florida Fish and Wildlif e Conservation Commi ssion. The collection

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of Sphyrna tudes in Trinidad would not have been possible without the gracious help and logistical support of Nichol as and Anthony Elias. Comp uted tomography scans and reconstructions would not have been possible without the help of Mason Dean and Mike Melendez. Erin Faltin, Dan Huber, Mari a Laura Habeggar, Samantha Mulvany, Dayv Lowry, Lisa Whitenack, Alpa Wintzer, Ste phen Deban, Jason Rhor, Theodore Garland Jr., and Enric Corts provided much needed discussion, editing, a nd stress relief during this project. Funding both for this project and to present this work to the broader scientific community was provided by the Department of Integrative Biology, the University of South Florida Student Governme nt, the University of South Florida, the American Elasmobranch Society, the Society for Integrative and Comparative Biology, the Porter Family Foundation, and a Nationa l Science Foundation grant to P.J.M (IOS – 0640133).

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i TABLE OF CONTENTS LIST OF TABLES .................................................................................................................. iii LIST OF FIGURES ...................................................................................................................v ABSTRACT ......................................................................................................................... vii GENERAL INTRODUCTION .....................................................................................................1 EVOLUTIONARY HISTORY OF SPHYRNID SHARKS .....................................................2 HYPOTHESIZED FUNCTIONS OF THE CEPHALOFOIL ...................................................3 FUNCTIONAL MORPHOLOGY AND CONSTRAINTS ......................................................5 FEEDING BIOMECHANICS ..........................................................................................7 GOALS ......................................................................................................................8 LITERATURE CITED .................................................................................................10 CHAPTER 1: CONSTRUCTIONAL CONSTRAINTS WITHIN THE HEAD OF HAMMERHEAD SHARKS (SPHYRNIDAE) .................................................................................................17 ABSTRACT ..............................................................................................................17 INTRODUCTION .......................................................................................................18 MATERIALS AND METHODS ....................................................................................22 Cephalofoil Shape ......................................................................................22 Electrosensory Pores ..................................................................................23 Internal Volumes ........................................................................................24 Statistics .....................................................................................................25 RESULTS .................................................................................................................27 Cephalofoil Shape ......................................................................................27 Electrosensory Pores ..................................................................................29 Internal Volumes ........................................................................................29 DISCUSSION ............................................................................................................32 External Shape Differences among Sphyrnids ..........................................32 Internal Cranial Volumes ...........................................................................37 Constructional Constrai nts within the Cranium .........................................39 The Ancestral Sphyrnid .............................................................................42 Evolution of the Cephalofoil ......................................................................43 CONCLUSIONS .........................................................................................................46 LITERATURE CITED .................................................................................................47

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ii CHAPTER 2: FUNCTIONAL MORPHOLOGY OF THE FEEDING APPARATUS IN HAMMERHEAD SHARKS (SPHYRNIDAE): A PHYLOGENETIC PERSPECTIVE. ....................77 ABSTRACT ..............................................................................................................77 INTRODUCTION .......................................................................................................78 MATERIALS AND METHODS ....................................................................................83 Volumetric Measures .................................................................................84 Feeding Morphology and Bite Fo rce Generation in Sphyrnids .................84 Statistical Analyses ....................................................................................86 RESULTS .................................................................................................................87 Feeding Morphology and Biomechanics ...................................................87 Changes among Feeding and Sensory Structures ......................................90 Ancestral State Reconstructions ................................................................92 DISCUSSION ............................................................................................................92 Feeding Morphology and Biomechanics ...................................................92 Changes among Feeding and Sensory Structures ....................................100 CONCLUSIONS .......................................................................................................104 LITERATURE CITED ...............................................................................................105 CHAPTER 3: BITE FORCE AND PERFORMANCE IN THE DUROPHAGOUS BONNETHEAD SHARK, SPHYRNA TIBURO. ..........................................................................................129 ABSTRACT ............................................................................................................129 INTRODUCTION .....................................................................................................130 MATERIALS AND METHODS ..................................................................................133 Experimental Animals .............................................................................133 Theoretical Bite Force..............................................................................134 Restrained Bite Force ...............................................................................135 Tetanic Bite Force ....................................................................................136 Performance Testing of Prey ...................................................................137 Statistical Analyses ..................................................................................138 RESULTS ...............................................................................................................139 Feeding Biomechanics and Bite Force ....................................................139 Performance Testing of Prey ...................................................................140 DISCUSSION ..........................................................................................................141 Feeding Biomechanics and Bite Force ....................................................141 Model Verification ...................................................................................143 Ecological Performance ...........................................................................144 CONCLUSIONS .......................................................................................................147 LITERATURE CITED ...............................................................................................148 OVERALL CONCLUSIONS ...................................................................................................164 ABOUT THE AUTHOR .............................................................................................. End Page

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iii LIST OF TABLES Table 1.1 Average volume (cm3) of the eye standard error measured using three different methods ........................................................................68 Table 1.2 Correlation matrix performe d on phylogenetically corrected data for sphyrnid and outgroup carcharhinid species ..................................69 Table 1.3 Average electrosensory por e counts standard error for both dorsal and ventral surfaces of the head ................................................71 Table 1.4 Average standard error for volumes for each internal element of hammerhead sharks and outgroup carcharhinids .................................72 Table 1.5 Correlation matrix perfor med on raw size-removed data for sphyrnid and outgroup carcharhinid species ........................................74 Table 1.6 Ancestral state reconstructi ons at each of the nodes along sphyrnid phylogeny (Figure 1)............................................................................76 Table 2.1 Average raw values s.e. for feeding morphology variables for sphyrnid and carcharhinid species .....................................................121 Table 2.2 Average raw volumes (cm3) s.e. for the cartilaginous elements of the feeding system of sphyrnid and carcharhinid species ..................124 Table 2.3 Percent contribution of each muscle to total force production among sphyrnid and carcharhinid species .........................................125 Table 2.4 Bite force among sphyrnid and outgroup carcharhinid species ...............126 Table 2.5 Correlation matrix of fe eding and head morphology data for sphyrnid and carcharhinid species .....................................................127 Table 2.6 Ancestral state reconstr uctions at each of the nodes along phylogeny (Figure 1)..........................................................................128 Table 3.1 Average force and mass standa rd error of the four principal jaw adducting muscles in S. tiburo ...........................................................160

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iv Table 3.2 Average maximum bite force (N) standard error for Sphyrna tiburo in each testing condition..........................................................161 Table 3.3 Comparison of absolute bite force and size-removed bite force residuals among fishes .......................................................................162 Table 3.4 Scaling of crab carapace prope rties with respect to length, width, depth, and mass ..................................................................................163

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v LIST OF FIGURES Figure 1.1 Phylogeny of the hammerhead sharks modified from Lim et al. (2010) ...................................................................................................55 Figure 1.2 External landmarks chos en for geometric morphometrics ........................56 Figure 1.3 Shape differences between C. acronotus (gray) and R. terraenovae (green) ..................................................................................................57 Figure 1.4 Shape differences between C. acronotus (gray) and E. blochii (green) ..................................................................................................58 Figure 1.5 Shape differences between E. blochii (gray) and S. mokarran (green) ..................................................................................................59 Figure 1.6 Shape differences between S. mokarran (gray) and S. zygaena (green) ..................................................................................................60 Figure 1.7 Shape differences between S. zygaena (gray) and S. lewini (green) ..........61 Figure 1.8 Shape differences between S. lewini (gray) and S. tudes (green) ..............62 Figure 1.9 Shape differences between S. tudes (gray) and S. tiburo (green) ..............63 Figure 1.10 Principal components analysis of head shape within carcharhinid and sphyrnid sharks..............................................................................64 Figure 1.11 Electrosensory pore maps overlain onto phylogeny ..................................65 Figure 1.12 Representative reconstructions of the internal elements of the head of hammerhead sharks overlain onto phylogeny .................................66 Figure 1.13 Chondrocranial struct ures of the cephalofoil of Eusphyra blochii ............67 Figure 2.1 Phylogeny of the hammerhead sharks modified from Lim et al. (2010) .................................................................................................115 Figure 2.2 Dorsal (a) and lateral (b) views of the cartilaginous elements within the cephalofoil of S. lewini .....................................................116

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vi Figure 2.3 Morphology of the feeding a pparatus shown on a reconstruction of S. lewini ..............................................................................................117 Figure 2.4 PCA plot of to tal length removed raw feeding morphology data ............118 Figure 2.5 Chondrocranim, mandibular, and hyoid arch skeletons of each species overlain onto phylogeny ........................................................119 Figure 2.6 Raw bite force among sphyrni d and closely related carcharhinid species ................................................................................................120 Figure 3.1 Feeding musculature of Sphyrna tiburo ...................................................154 Figure 3.2 Percent contribution of each feeding muscle to bite force .......................155 Figure 3.3 Typical crushing for ce curve for a 40.5 mm CL, 67.5 g C. sapidus crushed at a loading rate of ~370 mm/s using jaws removed from a 78.4 cm PCL S. tiburo ............................................................156 Figure 3.4 Blue crab, C. sapidus crushing results from fracture experiments on live crabs .......................................................................................157 Figure 3.5 Occurrence of blue crabs, C. sapidus in the stomachs of S. tiburo from Corts et al. (1996) ....................................................................158 Figure 3.6 Anterior and posterior m echanical advantages for durophagous chondrichthyans studied to date .........................................................159

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vii Evolution of the Hammerhead Cephalofoil: Shape Change, Space Utilization, and Feeding Biomechanics in Hammerhead Sharks (Sphyrnidae) Kyle Reid Mara ABSTRACT The relationship between form and function is often used to elucidate the biological role of a structure. Hammerhead sharks offer a unique opportunity to study form and function through phylogeny. Because sphyrni d sharks display a range of cranial morphologies this group can be used to addr ess questions about the evolution of cranial design and investigate the effects of change s in head morphology on feeding structures and bite force. Geometric morphomet rics, volumetric analyses, morphological dissections, and phylogenetic anal yses of the cephalofoil were used to gain insight into changes in cranial design th rough evolutionary history. External morphometrics and internal volumetric analyses indicated that while the external shap e of the cephalofoil and placement of the sensory structures is variab le through evolutionary history, the volumes of the internal cranial elements do not ch ange. Constructional c onstraints within the cephalofoil were confined to sensory stru ctures while feeding morphology remained relatively unchanged. Analysis of the morphology and biomechanics of the feeding apparatus revealed that th rough phylogeny the feeding system does not change among sphyrnid species. However, size-removed bite force was lower than predicted for all sphyrnid species except Sphyrna mokarran Despite differences in head morphology

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viii between sphyrnid and carcharhinid sharks, th e feeding bauplan is conserved in sphyrnid sharks with few changes to the feeding st ructures. Instead the chondrocranial and sensory structures are modified around the rela tively static feeding core. Finally, the durophagous S. tiburo was found to consume hard prey in a manner that is biomechanically and morphologically differe nt from other durophagous fishes. Furthermore, the diet of S. tiburo is constrained by the properties of its preferred prey.

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1 GENERAL INTRODUCTION Hammerhead sharks (Elasmobranchii, Ca rcharhiniformes, Sphyrnidae) are a unique group of cartilaginous fishes that possess a dorso-ventrally compressed and laterally expanded region of the head known as the cephalo foil. The cephalofoil is formed by lateral expansion and modification of the rostral, olfact ory, and optic regions of the chondrocranium (Compagno, 1984; 1988; Haenni, 2001). The degree of lateral expansion is variable through evolutionary history. Howeve r, it generally ranges from 18% of shark total length ( TL) in the bonnethead shark, Sphyrna tiburo to 50% of TL in, the aptly named, winghead shark, Eusphyra blochii Hammerhead fossil remains have been found in deposits dating to the Eocene (54.8 – 33.7 mya) (Gilbert, 1967). Sphyrnid sharks are circumglobal and ra nge from sea grass flats to open ocean continental shelf habitats (Compagno, 1984; 1988). The evolution of the peculiar he ad shape has been studied for the last ~50 years. However, just now are the selective pressures that govern the design of the cephalofoil beginning to be understood. With the creation of a robust multigene phylogeny for sphyrnid sharks (Lim et al., 2010), hammerhead sharks offer a unique opportunity for studying form and function in an historical context. Because the cephalofoil of sphyrnid sharks represents su ch a significant morphol ogical departure from the head morphology of their sister taxa, sphyrnids can be used as a morphological extreme from which to address questions a bout the evolution and functional trade-offs between feeding, sensory reception and neural structures (Herrel et al., 1999). And by interpreting form and functi on of a closely related group of organisms such as

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2 hammerhead sharks in an historical context we can gain a better understanding of the selective forces and constraints that govern the diversity of cranial form (Lauder and Liem, 1989; Herrel et al., 2001). EVOLUTIONARY HISTORY OF SPHYRNID SHARKS The phylogenetic relationship of hammerhead sharks indicates that the species with the most extreme lateral expansion of the cephalofoil ( Eusphyra blochii ) is the most basal while the least laterally expanded species ( Sphyrna tiburo ) is the most derived (Martin, 1993; Lim et al., 2010). Within the family Sphyrnidae there are two distinct genera ( Eusphyra and Sphyrna ) and eight currently recognized species ( E. blochii S. mokarran S. zygaena S. lewini S. corona S. media S. tudes and S. tiburo ) along with the possibility of some geminate species within S. lewini and S. tiburo (Compagno, 1988; Naylor, 1992; Martin, 1993; 1995; Duncan et al., 2006; Quattro et al., 2006). Recent phylogenetic work indicates that the extreme cephalic morphology is the result of divergent selection acting on the primitive cephalofoil. Once the cephalofoil had originated, divergent evolutio nary processes shaped lineage s differently resulting in expansion along one lineage ( Eusphyra ) and contraction along another ( S. tiburo ). Furthermore, species of similar body si ze do not form monophyletic groups. The scalloped hammerhead, S. lewini is more closely related to small species ( S. corona S, media S. tudes and S. tiburo ) than it is to other la rge circumglobal species ( S. mokarran and S. zygaena ). Ancestral body size reconstructions also indicate that the common ancestor to all sphyrnid sharks was most likely a large bodied (>150 TL) shark (Lim et al., 2010).

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3 HYPOTHESIZED FUNCTIONS OF THE CEPHALOFOIL There has been considerable debate as to the origin and biol ogical role of the cephalofoil (Tester, 1963; Thomson and Simanek, 1977; Compagno, 1984; Johnsen and Teeter, 1985; Strong et al., 1990; Marti n, 1993; Nakaya, 1995; Kajiura, 2001; 2003; Kajiura et al., 2003). A number of hypothese s have been put forth to explain the evolution of the cephalofoil. The hydrodynami c lift hypothesis states that the cephalofoil functions similarly to a canar d wing and provides hydrodynamic lif t at the anterior end of the animal, thereby increasing maneuverab ility (Nakaya, 1995; Driver, 1997). The sphyrnid cephalofoil is unique among elasmobranchs in that it has camber, possibly providing lift (Kajiura et al., 2003). Lift at th e anterior end of the body is also provided by the pectoral fins (Thomson and Sima nek, 1977; Wilga and Lauder, 2002). This hypothesis is supported by s phyrnids with larger heads having smaller pectoral fin areas, while the total area of the cephalofoil and pe ctoral fins remains constant among species (Thomson and Simanek, 1977; Compagno, 1984; Kajiura et al., 2003). Furthermore, when similar sized sharks are compared, sphyrn ids have much smaller pectoral fins than carcharhinids which lack a cepha lofoil (Nakaya, 1995; Driver, 1997). The cephalofoil may also function in prey manipulation (Strong et al., 1990; Chapman and Gruber, 2002). This hypothesis is based on two observations of a great hammerhead S. mokarran using its cephalofoil to stun and pin stingrays ( Dasyatis americana ) and eagle rays ( Aetobatus narinari ) to the seafloor. After restraining the rays, the hammerhead rotated its body so that it could bite off the pectoral fins (Strong et al., 1990; Chapman and Gruber, 2002).

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4 The remaining hypotheses concerning sphyr nid cephalofoil origins are based on changes in sensory biology as a result of in creased cranial surface area (Kajiura, 2003). The greater olfactory gradient resolution hypo thesis is based on the greater separation distance of the nares in sphyrnid sharks providing enhanced olfactory klinotaxis, increased olfactory acuity, and increased sampling area (Johnsen and Teeter, 1985). When bilateral and unilateral olfactory stimulation on live S. tiburo were performed, it was found that when a stimulus was applied to one nostril and not the other, bonnethead sharks initiated gradient searching behavi or (Johnsen and Teeter, 1985). More recent work suggests that the cephalo foil can provide enhanced klinotaxis indicating that hammerheads with larger heads have an increa sed ability to resolve odors across the head (Kajiura et al., 2005; Gardiner and Atema, 2010). Furthermore, the cephalofoil provides for a greater sampling area than carcharhinid sp ecies (Kajiura et al., 2005). However, the olfactory epithelia surf ace area does not differ between s phyrnid and carcharhinid sharks (Kajiura et al., 2005). A s econd hypothesis based on sensory biology is the enhanced binocular vision hypothesis (Tester, 1963). Th is hypothesis states that the placement of the eyes on the laterally expanded cephalofoil enhances binocular vision anteriorly and increases the visual field of sphyrnids (Tester, 1963; Comp agno, 1984; 1988). Recent work has show support for enha nced binocular overlap and a decreased blind area in the most laterally expanded species E. blochii and S. lewini (McComb et al., 2009). The hypothesis that is most commonly pr oposed concerning the evolution of the sphyrnid cephalofoil is the enhanced electrosensory hypothesis (Compagno, 1984; Kajiura, 2001). The basis for this hypothesis is the idea that the larger the surface area of the cephalofoil is, the greater the surface area that is devoted to electroreception,

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5 providing the shark with increased ability to detect and spatially resolve the bioelectric fields of prey (Compagno, 1984; 1988; Ka jiura, 2001; Brown, 2002; Kajiura and Holland, 2002). The laterally expanded head also enables sphyrnid sharks to possess ampullary tubules that are longer than thos e found in carcharhinid sharks (Chu and Wen, 1979) which may confer greater sensitivity to un iform electric fields th an their sister taxa (Murray, 1974; Bennett and Clusi n, 1978). Previous studies ha ve investigated and found varying degrees of support for these hypothese s individually (Nakay a, 1995; Kajiura and Holland, 2002; Kajiura et al., 2003; 2005; McComb et al., 2009). However, in order to understand the evolution and function of the hammerhead cephalofoil; sensory, neural, feeding, and morphological data must be investigated in concert. FUNCTIONAL MORPHOLOGY AND CONSTRAINTS Form and function relationships are of ten utilized to link an organism’s morphology with its ecological or biological role (Bock, 1980; Bock and von Wahlert, 1965). In order to truly unde rstand how an organism’s fo rm relates to its ecology, performance must be taken into account. Performance provides an estimate of an organism’s ability to accomplish ecologically re levant tasks such as prey consumption or the ability to escape predat ors (Irschick, 2002). Many such studies have drawn substantial conclusions regarding the relati onship been morphology and variables such as prey type, habitat, and community structur e (Herrel et al., 1996; Losos, 1992; Losos et al., 1994; Irschick and Losos, 1999; Korff a nd Wainwright, 2004; Toro et al., 2004). The study of vertebrate form-function co mplexes, such as the cranium, is incomplete unless is incorporates the constraints imposed by its constituent elements

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6 (Barel et al., 1989). Functiona l constraints can include ecolog ical constraints, behavioral constraints, physiological constraints, mo rphological constraints, and constructional constraints. Ecological cons traints include environmental factors and interspecific and intraspecific interactions such as competiti on. When the organism’s behavior imposes limits upon the use of a struct ure, the term behavioral constraints is utilized. Physiological constraints involve limitations of the sensory systems and physiological processes such as nutrient processing. Morphological constr aints result from constructional or architectura l limitations imposed upon a give n structure. Constructional constraints occur when spatial limitations are placed on a structure that has multiple biological roles (Barel, 1984; Reif et al., 1985; Motta and Kotrschal, 1992). These morphological constraints are sometimes referre d to as phylogenetic constraints if the trait remains static across a range of closel y related organisms (Sakamoto et al., 2010) Constructional constraints are particularly important when inve stigating the morphology of the spatially limited cranium. The cranium must contain all structures associated with feeding, respiration, neural integration, se nsory reception, and musculoskeletal support (Barel, 1983; 1984; Motta and Kotrschal, 1992; He rrel et al., 2000; De vaere et al., 2001). However, the various components within the cranium often impose constructional constraints and trade-offs in other stru ctures (Barel, 1983; 1984; Nijhout and Emlen, 1998; Devaere et al., 2001; Huber, 2006). Constraints have been previously demonstrated between and among sensory an d feeding structures (Barel, 1983; 1984; Devaere et al., 2001; Huber, 2006).

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7 FEEDING BIOMECHANICS The chondrichthyan feeding mechanism is markedly different from that of bony fishes in that they lack pharyngeal jaws and have skeletal structures composed of tessellated cartilage rather than bone. Despite this pliant skeletal material, at least eight groups of chondrichthyans are durophagous, or ha ve the ability to consume hard prey (Compagno et al., 2005; Huber et al., 2005; 2008; Ramsay and Wilga, 2007). In fishes, durophagy is often associated with enlarg ed jaw closing muscles, pavement-like molariform teeth, increased bite force, and fusion of the jaw symphysis (Wainwright, 1988; Turingan and Wainwright, 1993; Hern ndez and Motta, 1997; Clifton and Motta, 1998; Summers, 2000; Huber and Motta, 2004; Su mmers et al., 2004; Huber et al., 2005). These morphological modifications are often accompanied by behavioral modifications including unilateral biting, asynchronous musc le activity, tooth reorientation during biting, and specialized motor patterns (Su mmers, 2000; Wilga and Motta, 2000; Ramsay and Wilga, 2007). Hammerhead sharks use a number of tec hniques for capturing prey. The larger species rely primarily on ram feeding and consume fish (Clarke, 1971; Compagno, 1984; 1988; Stevens and Lyle, 1989; Wilga and Motta, 2000; Motta, 2004) while the smaller species use a combination of prey capture te chniques and consume a much wider array of prey species, ranging from crustaceans to fishes (Compagno, 1984; Wilga and Motta, 2000). A detailed examination of their feeding morphology, biom echanics, and prey capture behavior (kinematics) may reveal diffe rences among species as a result of dietary and prey capture characteristics.

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8 Despite the variation seen in feeding behavior and prey types in hammerhead sharks, feeding morphology and anatomy has b een described for only one of the eight extant species ( S. tiburo Wilga and Motta, 2000). Sphyrna tiburo is the most derived species of hammerhead and also shows the great est specialization of prey types, feeding primarily on portunid crabs in south Florid a (Compagno, 1984; Corts et al., 1996; Lessa and Almeida, 1998; Wilga and Motta, 2000; Be thea et al., 2007). Wilga and Motta (2000) found that S. tiburo exhibits very littl e upper jaw protrusion compared to other sharks and is the only hammerhead with mola riform teeth. The feed ing specialization of S. tiburo has resulted in morphological characters, su ch as molariform teeth, that separate it from other hammerheads. A detailed st udy of the cranial musculature of other hammerhead sharks is clearly needed before th e evolution of cranial form in this group can be understood (Wilga and Motta 2000). GOALS The goal of this study was to investig ate the evolution and function of the hammerhead cephalofoil and the consequences of changes in head shape and form on feeding morphology and sensory structures a nd to elucidate any pot ential cons tructional constraints between or among feeding and sens ory structures. For the first chapter, I utilized three-dimensional rec onstructions of the internal elements within the cephalofoil along with a recently publis hed phylogeny (Lim et al., 2010) and investigated any potential constructional constraints through e volutionary history. The specific goals for this portion of the study were to: 1) investig ate the shape changes of the sphyrnid head through phylogeny; 2) examine the volumetri c changes of cephalic elements through

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9 phylogeny; and 3) investigate potential construc tional constraints between and among feeding, neural and sensory structures. By interpreting form and function of a closely related group of organisms such as hammerhead sharks in an historical context a better understanding of the selective forces and constr aints that govern the evolution of cranial diversity can be obtained (Lauder an d Liem, 1989; Herre l et al., 2001). In the second chapte r, I investigated the functi onal morphology of the feeding apparatus in sphyrnid sharks. A study of the feeding mo rphology and biomechanics of this clade may provide a window into the se lective forces and constraints that govern cranial form in this unique group of very sp ecialized fishes. Becau se the cephalofoil of hammerhead sharks represents such a morphological departure from the head morphology found in other carcha rhiniform sharks, it can be used to address the evolution and consequences of changes in head form, and reveal functional morphological differences am ong species related to feeding. I utilized detailed anatomical dissections to ascertain the biom echanics of the feedi ng apparatus. This together with the output forces for each of the four principal jaw closing muscles was used in a three-dimensional st atic model of bite force (Hub er et al., 2005). These data were also investigated through phylogeny using appropriate phylogenetic comparative methods (Garland et al., 2005). The specific go als for this part of the study were to: 1) describe and compare the functional mo rphology and biomechanics of the feeding apparatus of the hammerhead sharks; 2) inve stigate if changes to the feeding bauplan exist in sphyrnid shark or if changes are confined to surrounding structures with conservation of the feeding apparatus; and 3) investigate the relationship between cranial design and feeding morphology within this clade.

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10 Lastly, I investigated further the en igma of durophagy in the bonnethead shark S. tiburo Sphyrna tiburo consumes hard prey (including swimming crabs Callinectes spp. and small lobsters Panulirus argus ) in south Florida (Compagno, 1984; Smith and Herrnkind, 1992; Corts et al., 1996; Lessa an d Almeida, 1998; Bethea et al., 2007). However, it does so without many of the mor phological specializations typically seen in durophagous chondrichthyans (Summers, 2000; Su mmers et al., 2004; Huber et al., 2005; Mara et al., 2010). Li ttle is known about how S. tiburo consumes hard prey without these specializations. The goals of this study were therefore to: 1) characterize the mechanical function of the feeding mechanism of S. tiburo through biomechanical modeling of biting and bite force measurements obtained via teta nic stimulation of jaw muscles and restraint of live animals; 2) compare the bite force of S. tiburo with that of other fishes; and 3) identify functional constraints on prey capture and diet by comparing the bite force of S. tiburo to the fracture properties of its primary prey item, blue crabs Callinectes sapidus LITERATURE CITED Barel, C. D. N. (1983). Towards a constructiona l morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology 33 357-424. Barel, C. D. N. (1984). Form-relations in the contex t of constructional morphology: the eye and suspensorium of lacustrine Ci chlidae (Pisces, Teleostei): with a discussion on the implications for phyloge netic and allometric form-interactions. Netherlands Journal of Zoology 34 439-502. Barel, C. D. N., Anker, C. C., Witte, F., Hoogerhoud, R. J. C., and Goldschmidt, T. (1989). Constructional constraint a nd its ecomorphological implications. Acta Morphologica Neerlando-Scandinavica 27 83-109. Bennett, M. V. L. and Clusin, W. T. (1978). Physiology of the ampulla of Lorenzini, the electroreceptor of elasmobranchs. In Sensory Biology of Sharks, Skates, and Rays Eds. E. S. Hodgson and R. F. Mathewson, pp. 483-505. Arlington, Virginia: Office of Naval Research.

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11 Bethea, D. M., Hale, L., Carlson, J. K., Co rts, E., Manire, C. A., and Gelsleichter, J. (2007). Geographic and ontogenetic variatio n in the diet and daily ration of the bonnethead shark, Sphyrna tiburo from the eastern Gulf of Mexico. Marine Biology 152 1009-1020. Bock, W. J. (1980). The definition and rec ognition of biological adaptation. American Zoologist 20 217-227. Bock, W. J. and von Wahlert, G. (1965). Adaptation and the form-function complex. Evolution 19 269-299. Brown, B. R. (2002). Modeling an electrosen sory landscape: behavioral and morphological optimization in el asmobranch prey capture. Journal of Experimental Biology 205 999-1007. Chapman, D. D. and Gruber, S. H. (2002). A further observation of the prey-handling behavior of the great hammerhead shark, Sphyrna mokarran : predation upon the spotted eagle ray, Aetobatus narinari Bulletin of Marine Science 70 947-952. Chu, Y. T. and Wen, M. C. (1979). Monograph of fishes of China (No. 2): a study of the lateral-line canal system and that of Lorenzini ampulla and tubules of elasmobranchiate fishes of China. Shanghai: Science and Technology Press. Clarke, T. A. (1971). The ecology of the scalloped hammerhead shark, Sphyrna lewini in Hawaii. Pacific Science 25 133-144. Clifton, K. B. and Motta, P. J. (1998). Feeding morphology, diet, and ecomorphological relationships among five Caribbean labrids (Teleostei, Labridae). Copeia 1998 953-966. Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shar k species known to data. Part 2. Carcharhiniformes. FAO Fish. Synop.: (125) Vol. 4, Pt. 2. Compagno, L. J. V. (1988). Sharks of th e order Carcharhiniforme s. Princeton: Princeton University Press. Compagno, L. J. V., Dando, M., and Fowler, S. (2005). Sharks of the world. Princeton, NJ: Princeton University Press. Corts, E., Manire, C. A., and Hueter, R. E. (1996). Diet, feedin g habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo in southwest Florida. Bulletin of Marine Science 58 353-367.

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12 Devaere, S., Adriaens, D., Verraes, W., and Teugels, G. G. (2001). Cranial morphology of the anguilliform clariid Channallabes apus (Gnther, 1873) (Teleostei: Siluriformes): are adap tations related to powerful biting? Journal of Zoology, London 255 235-250. Driver, K. H. (1997). Hydrodynamic properties and ecomorphology of the hammerhead shark (Family Sphyrnidae) cephalofoil ., pp. 159: Dissertation. University of California Davis, Davis, CA. Duncan, K. M., Martin, A. P., Bowen, B. W., and De Couet, H. G. (2006). Global phylogeography of the scalloped hamme rhead shark (Sphyrna lewini). Molecular Ecology 15 2239-2251. Gardiner, J. M. and Atema, J. (2010). The function of b ilateral odor arrival time differences in olfactory orientation of sharks. Current Biology, doi:10.1016/ j.cub.2010.04.053. Garland Jr., T., Bennett, A. F., and Rezende, E. L. (2005). Phylogenetic approaches in comparative physiology. Journal of Expe rimental Biology 208 3015-3035. Gilbert, C. R. (1967). A revision of the hammerh ead sharks (Family Sphyrnidae). Proceedings of the United States National Museum 119 1-88. Haenni, E. G. (2001). On the growth, func tional morphology, and embryological development of the cephalofoil in the bonnethead shark, Sphyrna tiburo ., pp. 253: Dissertation. Clemson Un iversity, Clemson, SC. Hernndez, L. P. and Motta, P. J. (1997). Trophic consequences of differential performance: ontogeny of oral jaw-cr ushing performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae). Journal of Zoology, London 243 737-756. Herrel, A., Cleuren, J., and De Vree, F. (1996). Kinematics of feeding in the lizard Agama stellio Journal of Experimental Biology 199 1727-1742. Herrel, A., Aerts, P., Fret, J., and De Vree, F. (1999). Morphology of the feeding system in agamid lizards: ecological correlates. The Anatomical Record 254 496507. Herrel, A., Aerts, P., and De Vree, F. (2000). Cranial kinesis in geckoes: functional implications. Journal of Expe rimental Biology 203 1415-1423. Herrel, A., De Grauw, E., and Lemos-Espinal, J. A. (2001). Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology 290 101107.

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13 Huber, D. R. (2006). Cranial biomechanics and feed ing performance of sharks., pp. 235. Dissertation. University of South Florida, Tampa, FL. Huber, D. R. and Motta, P. J. (2004). Comparative analysis of methods for determining bite force in the spiny dogfish Squalus acanthias Journal of Experimental Zoology 301A 26-37. Huber, D. R., Eason, T. G., Hueter, R. E., and Motta, P. J. (2005). Analysis of the bite force and mechanical design of the f eeding mechanism of the durophagous horn shark Heterodontus francisci Journal of Experimental Biology 208 3553-3571. Huber, D. R., Dean, M. N., and Summers, A. P. (2008). Hard prey, soft jaws and the ontogeny of feeding mechanics in the spotted ratfish, Hydrolagus colliei Journal of the Royal Society Interface 5 941-952. Irschick, D. J. (2002). Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integrative and Comparative Biology 42 278-290. Irschick, D. J. and Losos, J. B. (1999). Do Lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean Anoles. The American Naturalist 154 293-305. Johnsen, P. B. and Teeter, J. H. (1985). Behavioral respons es of bonnethead sharks ( Sphyrna tiburo ) to controlled olfactory stimulation. Marine Behaviour and Physiology 11 283-291. Kajiura, S. M. (2001). Head morphology and elect rosensory pore distribution of carcharhinid and sphyrnid sharks. Environmental Biology of Fishes 61 125-133. Kajiura, S. M. (2003). Electroreception in neonatal bonnethead sharks, Sphyrna tiburo Marine Biology 143 603-611. Kajiura, S. M. and Holland, K. N. (2002). Electroreception in juvenile scalloped hammerhead and sandbar sharks. Journal of Experimental Biology 205 26092621. Kajiura, S. M., Forni, J. B., and Summers, A. P. (2003). Maneuvering in juvenile carcharhinid and sphyrnid sharks: the role of the hammerhead shark cephalofoil. Zoology 106 19-28. Kajiura, S. M., Forni, J. B., and Summers, A. P. (2005). Olfactory morphology of carcharhinid and sphyrnid sharks: does the cephalofoil confer a sensory advantage? Journal of Morphology 264 253-263.

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14 Korff, W. L. and Wainwright, P. C. (2004). Motor pattern control for increasing crushing force in the striped burrfish ( Chilomycterus schoepfi ). Zoology 107 335346. Lauder, G. V. and Liem, K. F. (1989). The role of historical factors in the evolution of complex organismal functions. In Complex Organismal Functions: Integration and Evolution in Vertebrates Eds. D. B. Wake and G. Roth, pp. 63-78. New York: John Wiley & Sons, Ltd. Lessa, R. P. and Almeida, Z. (1998). Feeding habits of the bonnethead shark, Sphyrna tiburo from Northern Brazil. Cybium 22 383-394. Lim, D. D., Motta, P., Mara, K., and Martin, A. P. (2010). Phylogeny of hammerhead sharks (Family Sphyrnidae) inferred from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 55 572-579. Losos, J. B. (1992). The evolution of convergent structure in Caribbean Anolis communities. Systematic Biology 41 403-420. Losos, J. B., Irschick, D. J., and Schoener, T. W. (1994). Adaptation and constraint in the evolution of specialization of Bahamian Anolis lizards. Evolution 48 17861798. Mara, K. R., Motta, P. J., and Huber, D. R. (2010). Bite force and performance in the durophagous bonnethead shark, Sphyrna tiburo Journal of Experimental Zoology Part A. Ecological Genetics and Physiology 313 95-105. Martin, A. (1993). Hammerhead shark origins. Nature 364 494. Martin, A. P. (1995). Mitochondrial DNA sequence evol ution in sharks: rates, patterns, and phylogenetic inferences. Molecular Biology and Evolution 12 1114-1123. McComb, D. M., Tricas, T. C., and Kajiura, S. M. (2009). Enhanced visual fields in hammerhead sharks. Journal of Experimental Biology 212 4010-4018. Motta, P. J. (2004). Prey capture behavior and feed ing mechanics of elasmobranchs. In Biology of sharks and their relatives Eds. J. Carrier J. Musick and M. Heithaus, pp. 165-202. Boca Raton: CRC Press LLC. Motta, P. J. and Kotrschal, K. M. (1992). Correlative, experimental, and comparative evolutionary approaches in ecomorphology. Netherlands Journal of Zoology 42 400-415. Murray, R. W. (1974). The ampulae of Lorenzini. In Handbook of sensory physiology Ed. A. Fessard. New York: Springer-Verlag.

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15 Nakaya, K. (1995). Hydrodynamic function of the head in the hammerhead sharks (Elasmobranchii: Sphyrnidae). Copeia 1995 330-336. Naylor, G. J. P. (1992). The phylogenetic relationshi ps among requiem and hammerhead sharks: inferring phylogeny when thousands of equally most parsimonious trees result. Cladistics 8 295-318. Nijhout, H. F. and Emlen, D. J. (1998). Competition among body parts in the development and evolution of insect morphology. Proceedings of the National Academy of Sciences of th e United States of America 95 3685-3689. Quattro, J. M., Stoner, D. S., Driggers, W. B., Anderson, C. A., Priede, K. A., Hoppmann, E. C., Campbell, N. H., Duncan, K. M., and Grady, J. M. (2006). Genetic evidence of cryptic speciation within hammerhead sharks (genus Sphyrna ). Marine Biology 148 1143-1155. Ramsay, J. B. and Wilga, C. D. (2007). Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks ( Chiloscyllium plagiosum ). Journal of Morphology 268 664-682. Reif, W. E., Thomas, R. D. K., and Fischer, M. S. (1985). Constructional morphology: the analysis of cons traints in evolution. Acta Biotheoretica 34 233-248. Sakamoto, M., Lloyd, G. T., and Benton, M. J. (2010). Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance. Journal of Evolutionary Biology 23 463-478. Smith, K. N. and Herrnkind, W. F. (1992). Predation on early juvenile spiny lobsters Panulrus argus (Latreille): influence of size and shelter. Journal of Experimental Marine Biology and Ecology 157 3-18. Stevens, J. D. and Lyle, J. M. (1989). Biology of three hammerhead sharks ( Eusphyra blochii, Sphyrna mokarran, and S. lewini) from northern Australia. Australian Journal of Marine and Freshwater Research 40 129-146. Strong Jr., W. R., Snelson, F. F., and Gruber, S. H. (1990). Hammerhead shark predation on stingrays: an obs ervation of prey handling by Sphyrna mokarran. Copeia 1990 836-840. Summers, A. P. (2000). Stiffening the stingray skel eton an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). Journal of Morphology 243 113-126. Summers, A. P., Ketcham, R. A., and Rowe, T. (2004). Structure and function of the horn shark ( Heterodontus francisci ) cranium through ontogeny: development of a hard prey specialist. Journal of Morphology 260 1-12.

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16 Tester, A. L. (1963). Olfaction, gestation and the comm on chemical sense in sharks. In Sharks and Survival Ed. P. W. Gilbert, pp. 255-285. Boston: C.C. Heath and Company. Thomson, K. S. and Simanek, D. E. (1977). Body form and locomotion in sharks. American Zoologist 17 343-354. Toro, E., Herrel, A., and Irschick, D. (2004). The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. American Naturalist 163 844-856. Turingan, R. G. and Wainwright, P. C. (1993). Morphological and functional bases of durophagy in the queen triggerfish, Balistes vetula (Pisces, Tetraodontiformes). Journal of Morphology 215 101-118. Wainwright, P. C. (1988). Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69 365-645. Wilga, C. D. and Motta, P. J. (2000). Durophagy in sharks : feeding mechanics of the hammerhead Sphyrna tiburo Journal of Experimental Biology 203 2781-2796. Wilga, C. D. and Lauder, G. V. (2002). Function of the he terocercal tail in sharks: quantitative wake dynamics during stea dy horizontal swimming and vertical maneuvering. Journal of Experimental Biology 205 2365-2374.

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17 CHAPTER 1: CONSTRUCTIONAL CONSTRAINTS WITHIN THE HEAD OF HAMMERHEAD SHARKS (SPHYRNIDAE) ABSTRACT The biological role of an anatomical st ructure can be elucidated by investigating the relationship between form and function. The study of constructional constraints is particularly important if a structure, such as the cranium, serves multiple biological roles, and is therefore shaped by multiple selective pressures. The sphyrnid cephalofoil presents an excellent model for investigating potential trade-offs between sensory, neural, and feeding structures. In this study, hammer head shark species were chosen to represent differences in head form through phylogeny. A combination of surface-based geometric morphometrics, computed tomography volum etric analysis, and phylogenetic analyses were utilized to investigate potential tradeoffs within the head. Geometric surface landmark analyses indicate relative change s in the sensory stru ctures through phylogeny with few changes in the feeding appara tus. The more basal winghead shark Eusphyra blochii has small anteriorly positioned eyes. Through phylogeny the relative size and position of the eyes changes, such that derived species have larger, more medially positioned eyes. The lateral position of the external nares is highly variable, showing no phylogenetic trend. Mouth size and pos ition are conserved, remaining largely unchanged. Volumetric computed tomography (C T) analyses, however, reveal that there are subtle changes associated with the evol ution of the cephalofoil. The volume of the

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18 feeding muscles and jaw cartilages are positiv ely correlated through evolutionary history. The few constraints that were found were is olated to the nasal capsule volume’s inverse correlation with braincase, chondrocranial, and total cephalofoil volume. Eye volume was also constrained by increasing head widt h and decreasing depth of the cephalofoil. These data indicate that much of the head is morphologically conserved through sphyrnid phylogeny, particularly the jaw cartilages and their associated feed ing muscles, with shape change and constructional constraints be ing primarily confined to the lateral wings of the cephalofoil and its associated sensor y structures. Ancestr al charac ter state reconstructions agree with previous analyses that the common ancestor to all hammerhead sharks was large bodied with a relatively large laterally expanded head. INTRODUCTION The relationship between form and function can be used to reveal the biological role of a feature (Bock, 1980; Bock and von Wahlert, 1965). The study of this relationship, functional morphol ogy, has received considerable attention with regards to understanding feeding in fishes (reviewed by Lauder, 1980). By interpreting form and function of phylogenetically closely relate d organisms, a better understanding of the selective forces and constraint s that govern their diversity may be obtained. The study of vertebrate form-function complexes, such as the cranium, is incomplete unless it incorporates the constraints imposed by its constituent elements (Barel et al., 1989; Lauder and Liem, 1989; Herrel et al., 1999; 2000; Devaere et al., 2001; 2005). Constructional constraints occur when spat ial limitations are placed on a structure that has multiple biological roles (Barel, 1983; 1984; Reif et al., 1985; Motta and

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19 Kotrschal, 1992). When investigating th e functional morphology of the cranium, constructional constraints and spatial limitations are particularly important because a finite number of components can be contained within this morphospace. These components include structures associated with feeding, resp iration, neural integration, sensory reception, and musculoskeletal suppor t (Barel, 1983; 1984; Motta and Kotrschal, 1992; Herrel et al., 2000; Devaere et al., 2001). In anguilliform catfishes, hypertrophy of the adductor mandibulae complex results in neur ocranial narrowing a nd the reduction of some cranial bones. This reduction is due, in part, to spatial constraints resulting in tradeoffs between muscle mass and skeletal morphol ogy (Devaere et al., 2001). Horn size of dung beetles was found to impose trade-offs on the size of nearby st ructures, including the eyes and wings (Nijhout an d Emlen, 1998; Emlen, 2001). It should also be noted that constraints can occur in body part s that are distantly placed if these body parts rely on a common resource (Moczek and Nijhout, 2004). The co-constraints imposed between sensory and feeding structures is of partic ular importance when they occupy adjoining morphological space. Furthermore, head construction is primarily determined by sense organs which are affected by changes in othe r structures within th e head (Barel, 1983; Dullemeijer, 1958; 1974). Development of the brain is constrained by the position of the nasal capsule and eyes in ray-finned fish es (Striedter and Northcutt, 2006). Developmental trade-offs have also been shown between the extrinsic eye musculature and the musculature of the feeding appara tus in developing quail embryos (von Scheven et al., 2006). Changes in size of either sensory or feeding structures may impose functional trade-offs in the other (Barel et al., 1989; Patek and Oakley, 2003; Huber, 2006). In cichlid fishes, increasing eye si ze results in a concomitant decrease in

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20 suspensorium size and displacement of the adductor mandibulae (Barel et al., 1989; Liem, 1991). Other studies have found a lack of constraints between the volume of the adductor mandibulae muscle complex and the eye in cichlid fishes (Hulsey et al., 2007). Hammerhead shark heads (Elasmobranchii, Sphyrnidae) offer a unique opportunity for studying the relationship of form and function and constraints among sensory, neural, and feeding structures. Hammerheads ha ve a unique dorso-ventrally compressed and laterally expanded cephalofoil, da ting back to their origin in the Eocene (54.8-33.7 mya) (Gilbert, 1967). The cephalofoil is formed by lateral expansion of the rostral, olfactory, and optic regions of th e chondrocranium (Gilbert, 1967; Haenni, 2001). The shape of the cephalofoil ranges fr om extremely wide, in the case of Eusphyra blochii – 40-50% of total length (TL), to only moderately expanded, as seen in Sphyrna tiburo – 18-25% of TL (Compagno, 1984). Despite differences in lateral expansion, the volume of the head relative to TL remains uncha nged within hammerheads (Kajiura, 2001). Hammerhead sharks share a common ances try with carcharhinid sharks (Compagno, 1988; Naylor, 1992; Martin, 1993), with the mo st recent molecular da ta indicating that the hammerhead shark with the most expanded cephalofoil, E. blochii represents the most ancestral form, and the species with the least lateral expansion, S. tiburo is the most derived (Figure 1.1) (Lim et al., 2010; Martin, 1993). The unique head morphology found in this group of fishes raises questions about the distribution of both sensory and feeding elements throughout evolutionary hist ory and any concomitant trade-offs that may occur. Numerous, non-exclusive, hypotheses concer ning the evolution of the cephalofoil have been posited. Sensory hypotheses focu s on the cephalofoil providing an advantage

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21 due to the lateral expansion of the head a nd the resulting redistri bution of the sensory structures. These hypotheses include the enha nced binocular vision hypothesis (Tester, 1963b; Compagno, 1984; 1988), the greater ol factory gradient resolution hypothesis (Tester, 1963a; Johnsen and Teeter, 1985; Compagno, 1984; 1988; Kajiura et al., 2005), and the enhanced electrosensory hypothe sis (Compagno, 1984; Kajiura, 2001). Conversely, the cephalo foil may provide hydrodynamic lift a nd act as an anterior lifting body as stated in the hydr odynamic lift hypothesis (Thomson and Simanek, 1977; Compagno, 1984; Nakaya, 1995; Driver, 1 997; Kajiura et al., 2003). Lastly, hammerhead sharks have been observed on two separate occasions using their laterally expanded head to pin and restrain prey agai nst the bottom leading to the final hypothesis, the prey manipulation hypothesis (Strong et al., 1990; Chapman and Gruber, 2002). The possibility of constructional constr aints within the sphyrnid chondrocranium becomes paramount when considering that the relative volume of the sphyrnid shark cranium does not differ from that of carcharhi nid sharks (Kajiura, 2001 ). This indicates that the depressed cephalofoil of sphyrnid sh arks may result in sp atial changes in the surrounding structures and thereby impose spatial constraints on the constructional morphology of the sensory and feeding structur es (Herrel et al., 2000; Devaere et al., 2005). A similar situation in the depressed skull of the clariid catfish Platyallabe tihoni results in the gill and suprabranchial appa ratuses competing for space within the head which may have lead to the lo ss of the suprabranchial orga n (Devaere et al., 2001; 2005). Because the head of sphyrnid sharks repr esents such a significant morphological departure from the head morphology of their sister taxa, sphyrnids can be used as a morphological extreme from which to address questions about the e volution of functional

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22 constraints between feeding and sensory r eception (Nijhout and Emlen, 1998; Herrel et al., 1999; Emlen, 2001). Geometric morphometrics indicate that ontogenetic and evolutionary changes in sphyrnid head shape are not solely the result of lateral expansion of the head but involve modification of the entire cranium (Caval canti, 2004). However, this study only encompassed four of the eight sphyrnid sp ecies and did not include the most basal hammerhead, E. blochii The goals of this study were to 1) investigate the shape changes of the sphyrnid head through phylogeny; 2) examine the volumetric changes of cephalic elements through phylogeny; and 3) investig ate potential constructional constraints between and among feeding, neural, and sensor y structures. By in terpreting form and function of a closely related group of organisms, such as hammerhead sharks, in an historical context, a better understanding of the selective fo rces and constraints that govern the diversity of cranial design can be obtained (Lauder and Liem, 1989; Herrel et al., 2001). MATERIALS AND METHODS Cephalofoil Shape The external shape of the cephalofoil a nd chondrocranium was investigated with landmark-based geometric morphometrics (Book stein, 1996a; b; Adams and Rohlf, 2000; Trapani, 2003). The ventral surface of the head s from three to five mature individuals of each of six extant sphyrnid species repres enting differences in head shape and size through phylogeny ( Eusphyra blochii (Cuvier, 1816), Sphyrna mokarran (Rppel, 1837), S. zygaena (Linnaeus, 1758), S. lewini (Griffith and Smith, 1834), S. tudes

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23 (Valenciennes, 1822), S. tiburo (Linnaeus, 1758) and two fusiform carcharhinid shark outgroups ( Carcharhinus acronotus (Poey, 1860), and Rhizoprionodon terraenovae (Richardson, 1836)) were digitally phot ographed (Canon Powershot A710, Canon USA Inc. Lake Success, NY, USA). Eusphyra blochii were obtained from local fishers in Darwin Australia, S. mokarran and S. lewini were obtained from longline sampling and local anglers from the western and eastern peninsula of S. Florida, S. zygaena were obtained from the east coast of New Zealand, the western coast of Mexico, and the east coast of S. Florida, S. tudes were collected from local fish ers along the northeast coast of Trinidad, and S. tiburo C. acronotus and R. terraenovae were obtained from the waters of the Gulf of Mexico off Sarasota, Florida. Biologically significant points representing mouth, eye, incurrent and excurrent nare s (hereafter nares) position, and overall cephalofoil shape on the left side of the vent ral surface of the cephalofoil were digitized using TpsDig Software (F. J. Rohlf) (Figur e 1.2). After digiti zation, CoordGen (H.D. Sheets, Integrated Morpho metrics Package (IMP)) was used to produce Bookstein Coordinates with landmarks one and nine being used as the ba seline (Bookstein, 1991, 1996a; b). Procrustes superimposition was then used to realign the coordinates so that the centroids of all the landmarks for each species overlaped, reducing variance and effectively removing size (Lele and Ri chtsmeier, 2001; Kassam et al., 2003). Electrosensory Pores The dorsal and ventral cephalofoil skin was removed from each individual anterior to the posterior margin of the jaws. The underlying connective and muscle tissues were then dissected away from the sk in. The skins were th en placed between two sheets of glass and backlit. Digital pictures were then taken of the electrosensory pores

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24 and a composite image was created in A dobe Photoshop CS3 (Adobe Systems Inc. San Jose, CA, USA) by overlapping the images. Th e total number of pores on both the dorsal and ventral surface was counted and pore maps created using the NIH imaging software Image J v1.42. Internal Volumes Fresh frozen individuals of R. terraenovae (N = 3, 82.8 – 89.7 cm TL), C. acronotus (N = 3, 93.5 – 107.5 cm TL), E. blochii (N = 3, 133.8 – 165.6 cm TL), S. mokarran (N = 3, 210 – 249 cm TL), S. lewini (N = 3, 255 – 262.8 cm TL), S. zygaena (N = 2, 232 – 293 cm TL), S. tudes (N = 3, 69.3 – 102 cm TL), and S. tiburo (N = 3, 88.5 – 95 cm TL) were used for internal vol ume measurements. Each specimen was individually scanned with a 64 slice A quilion Toshiba (Toshi ba America Medical Systems Inc., Tustin, CA, USA) computed to mography (CT) scanner at a slice thickness of 0.5 – 1.0 mm. Computed to mography images for each individual were imported into AMIRA v4.1.2 software (Visage Imaging, Inc ., San Diego, CA, USA) and digitally reconstructed. Internal volumes of feed ing elements (hyomandibula, ceratohyal, basihyal, Meckel’s cartilage, and palatoquadrat e cartilage), sensory and neural structures (eye, internal nasal capsule, internal olfactory tract, and internal braincase), and chondrocranial elements (all remaining non feedi ng cartilages in the head, anterior to the posterior margin of the ceratohyal) were computed. Pharyngeal cartilages were consequently not considered nor were vertebral elements. Each element was selected from the appropriate CT slices to give accura te 3D geometry in the reconstructed head. Using the posterior-most point of the ceratohy al as a landmark, the total volume of the head was also computed. Volume computa tions were tested for accuracy by computing

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25 the volumes of eyes from R. terraenovae E. blochii S. lewini and S. tiburo Eye volume was digitized first from CT scans of whole h eads. Eyes were then unilaterally removed from each individual and CT scanned a second time outside of the animal. Finally, the water displacement volume was determined for each eye. The different methods of eye volume measurement were then compared using a one-way ANOVA. No significant differences were found among treatments (p = 0.08), and all further digitized volumes were assumed to be accurate (Table 1.1). The feeding muscles involved in lower jaw adduction: quadrotomandibularis ventral (Q MV), quadratomandibularis dorsal (QMD), preorbitalis ventral (POV), and preorbitalis dorsal (POD) (Wilga and Motta, 2000), were unilaterally excised and volume determined by water displacement. The volume of bilaterally symmetrical elements was mu ltiplied by two to account for both sides. Statistics Species geometric morphometric data were tested for significant differences with pairwise comparisons using G oodall’s F-test. Principal co mponents analysis (PCA) of head shape differences among species was ge nerated using PCAGen (IMP). Finally, in order to visualize the change s in shape among species, thin-p late splines were generated using IMP. Pore counts were compared among species using three separate Kruskal-Wallis one-way ANOVAs on ranks. Dorsal and ventral pore fields were first compared within species, next dorsal and ventral pore fields were compared among species. Raw volumes for the internal elements for all species were log transformed to account for the large size range among species and then input into a PCA to determine which variable(s) created separation among species and to reduce the number of

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26 variables. Principal components were not c onsidered to account for a significant amount of the variation unless their eigenvalue was gr eater than 1. Variables which were found to load heavily on a given principal compone nt (loading score gr eater than 0.6) were retained for further analysis. Initia lly, volumetric and pore data were log10 transformed and linearly regressed against log10 TL. Studentized residual s were then input into a Pearson correlation analysis to investigate relationshi ps among the size removed variables. Following this the most recent phylogeny with branch lengths for hammerheads (Lim et al., 2010; Martin, 1993) was used to generate independent contrasts for each of the raw morphologica l volumes, pore data, head width (HW), and shark TL using Mesquite v2.72 (Maddison and Maddison, 2009). The method of generating independent contrast s has been previously descri bed (Garland et al., 2005). Mesquite was used to determine if the br anch lengths of the phylogeny and model of evolution adequately fit the tip taxa data. Th e tree used here (Lim et al., 2010) was found to adequately fit the data of the extant taxa Positivised contrasts were then exported and independent contrasts were calc ulated by dividing the raw cont rast for each variable by its standard deviation. Th e independent contrasts method transforms the original phylogenetically non-independent data set in to a set of independent and equally distributed contrasts (Felsenste in, 1985). These contrasts re present rates of change along each branch of phylogeny. By ut ilizing this method the relatedness of ta xa within a study can be removed resulting in phylogenetical ly removed comparisons (Garland et al., 2005). Since the currently accepted phylogeny has only one outgroup species, C. acronotus was used as the outgroup for phylogeneti c analyses. The contrasts of each

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27 variable were then regressed through the orig in against the contrast of TL to remove the effect of size (Felsenstein, 1985). These phyl ogenetically corrected studentized residuals were then input into a Pearson correlation analysis, through the origin, to investigate relationships among the size and phylogeneticall y removed variables. Regressions, PCA analysis, and ANOVAs were performed in SYSTAT v11 (SYSTAT Software Inc., Chicago, IL, USA), and the correlation an alysis was performed in SPSS v18 (SPSS, Chicago, IL, USA). Additiona lly, Mesquite was used to perform ancestral state reconstructions using parsimony for each of the phylogenetically corrected variables to investigate how variables change through evolu tionary history. Each variable is traced backward through evolutionary history yielding character st ates at each node. These calculated character states are then used to calculate deeper nodes within the phylogeny. All procedures followed the Institutional Animal Care and Use Committee guidelines of Mote Marine Laboratory (0810-RH1, 07-10-PM1) and the Un iversity of South Florida (T3198, R3205, W3514). RESULTS Cephalofoil Shape Geometric morphometric analysis revealed that all species were significantly different from each other (p < 0.001). For ease of visualization, only shape changes on the left side of the shark are presen ted. Within the carcharhinid species, R. terraenovae differs from C. acronotus by having anteriorly positio ned eyes and incurrent and excurrent nares and anterior rostral expansion. Furthermore, the mouth is expanded and shifted anterolaterally in R. terraenovae compared to C. acronotus (Figure 1.3).

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28 Shape changes throughout the species are reflected by movement of the nares, eyes and cephalofoil, with relatively li ttle repositioning of the mouth. Between carcharhinid and sphyrnid sharks the head e xpanded laterally, forming the cephalofoil. As a result, the eyes and nares were also carried laterally. Mouth position remained relatively constant with sli ght posteromedial movement (F igure 1.4). Pairwise shape comparisons within sphyrnid sharks do not necessarily reflect ancestral shape changes, only the differences between extant taxa (Fi gure 1.1). Furthermore, the interpretation of shape differences between tip taxa will di ffer slightly with changes in topology. However, overall general trends will remain unchanged. When E. blochii is compared to S. mokarran cephalofoil expansion decreased and ey e position shifted anteriomedially in S. mokarran Nares position shifted anteriorly while mouth position shifted slightly posteriorly (Figure 1.5). Among S. mokarran S. zygaena and S. lewini there were few changes in overall cephalofo il shape. However, eye and nares position is first placed posterolaterally in S. zygaena compared to S. mokarran and then anteriorly in S. lewini compared to S. zygaena and again, mouth position remained mostly invariant (Figure 1.6 and 1.7). Differences in head shape between S. lewini and S. tudes were centered around decreased lateral expansion with slight rostral anterior expansion in S. tudes with almost no change in mouth position. Furthermore, both the eyes and nares are positioned anteromedially in S. tudes compared to S. lewini (Figure 1.8). Finally, S. tiburo displays decreased cephalofoil expansi on laterally and increased expa nsion rostrally compared to S. tudes Eye and nares position both shifted medially, while mouth position remained unchanged in S. tiburo (Figure 1.9). Principal components analysis of the geometric morphometric data shows separation along PC1, (78.8 % of the va riation) based on

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29 degree of lateral head expansion and PC2, ( 13.5% of the variation) based on placement of the nares and eyes. Eusphyra blochii is distinguished from th e remaining species by its extreme lateral expansion, the anterior position of the eyes on the lateral tips of the cephalofoil and the medial posi tion of the nares. Similarly, S. mokarran S. zygaena S. lewini and S. tudes group together based on their mode rate head expansion and laterally placed nares (Figure 1.10). Electrosensory Pores The number of dorsal pores was positively correlated with the number of ventral pores. Dorsal pore number was also correlated with increased head width. Pore numbers did not display correlated changes with any other cranial structure through evolutionary history (Table 1.2). The species w ith the largest number of pores was S. lewini however S. tudes a species with a less laterally expande d cephalofoil, had a similar number of pores (Table 1.3). Only C. acronotus S. mokarran and S. lewini had a greater number of ventral pores than dorsal (Table 1.3). Th e distribution of pores among the species was relatively consistent but species specific patterns are clearl y recognizable (Figure 1.11). Surprisingly, E. blochii had few pores distributed al ong both the dorsal and ventral anterior edge of the cephalofoil compared to the other species. Internal Volumes In general, the spatial orga nization of the central core of the chondrocranium (e.g. neurocranium, rostral cartilages, and feeding system) remains constant despite the various changes in cephalofoil shap e and size (light green, Figu re 1.12). The position and volume of the internal sensory structures and their associated cartilages (e.g. nasal capsule, eye, and olfactory tract) are vari able through phylogeny (Fi gure 1.12, Table 1.4).

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30 The nasal capsule expands laterally as a result of the extreme lateral expansion seen in basal sphyrnids. The prea nd post-optic cartila ges are reorganized to accommodate lateral displacement of the eyes and ex trinsic eye musculature (Figure 1.13, see Compagno, 1988). The position an d orientation of the jaws and suspensory cartilages remains relatively constant through phylogeny. Position and spatial organization of sensory structures displays noticeable differences thr ough phylogeny. Eye volume is particularly striking with basal species having relatively smaller eyes (Figure 1.12). That the number of correlations di ffers between the non-phylogenetically corrected and phylogenetically co rrected data demonstrates th at the data have a clear phylogenetic signal (Table 1.2 compared to Ta ble 1.5). As a result of the phylogenetic signal demonstrated by this data set, on ly phylogenetically corr ected data will be discussed further. Pearson correlation analyses revealed that changes to most elements within the head are not correlated with change s in the remaining elements (Table 1.2 p > 0.05). As the number of correlations increases the chance of spurious correlations increases (Aldrich, 1995). Because of this, only biologically relevant correlations that occur between adjacent structures will be di scussed further. However, some elements showed significant parallel patterns of change indicating that as one structure increases in size; other structure(s) show a concomitant increase in size. This is particularly apparent in the feeding muscles (QMV, QM D, POV, and POD) and the jaw and jaw suspension cartilages (palatoqu adrate cartilage, Meckel’s cartilage, hyomandibula, and ceratohyal). As the jaw cartilages increase in volume, the muscles that reside upon them also increase in volume (p < 0.025 Table 1.2). Furthermore, as one jaw closing muscle increased in volume, the remaining three muscle s also increased in volume. Similarly, as

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31 the volume of one jaw cartilage increased, the volume of the remaining jaw and the hyomandibula cartilages increas ed. Other positive trends dealt with increasing total volume being correlated with increased chondrocranial and braincase volume. Finally, there was a positive correlati on between head width and chondrocranial volume (Table 1.2). Negative correlations were found indicati ng an inverse relati onship. As nasal capsule volume increases, there is a conc omitant decrease in braincase, basihyal, chondrocranium, and total volume. Head widt h was also found to negatively affect the volume of the eye (p < 0.039 Table 1.2, Figure 1.12). Ancestral state reconstructions indicate that the closest an cestor of sphyrnid sharks was intermediate in length between large and sm all bodied hammerhead sharks (~177.49 cm TL) and similar to large bodied shar ks in extent of lateral head expansion (47.45 cm or ~26.9% of TL). Meckel’s cart ilage volume was found to be greater than palatoquadrate volume as is seen in all ex tant species (Table 1.4 and 1.6, Figures 1.1 and 1.12, Node 3). The volume of the QMV and P OV was greater than the remaining feeding muscles. This trend is mirrored in extant sphyrnids but not outgroups (Table 1.4). Despite the changes in volume of the vari ous elements, electrosensory pore counts remained relatively consistent through evol utionary history (Table 1.6) as does the general spatial organization of the electrosensory system (Figure 1.11).

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32 DISCUSSION External Shape Differences among Sphyrnids All species studied had sign ificantly different head shapes. The shape of the cephalofoil has long been used to visually distinguish species of hammerhead shark (Compagno, 1984; 1988). The morphology behind these shape differences has remained largely unknown. Cavalcanti ( 2004) correctly concluded that the changes within the sphyrnid head are the result of modifications to almost all chondrocranial elements and not simply the result of expanding the head laterally. While the geometric morphometric analysis of the current st udy also reveals the underlying pattern of change in the chondrocranial elements, the placement of the eyes, nares, and mouth on the cephalofoil and how their placement changes among species is of particular interest. Eye position is variable through phylogeny (yello w lines, Figures 1.3 1.9). Furthermore, the eyes are not consistently laterally pl aced on the cephalofoil. In E. blochii and S. lewini the eyes are positioned at the anterior edge of the dist al tip of the cephalofoil, while in all other species the eye is more posteriorly placed. In order to accommodate lateral placement of the eyes, the preand post-orbital pro cesses are highly modified (Compagno, 1988; Schultze, 1993) (Figure 1.12 and 1.13). The postorbital process is pa rticularly affected by differences in head shape. In E. blochii, the post orbital process is much more gracile than in the remaining species, due in part to the extreme lateral expansion seen in this species (Figure 1.13). Given the lateral expansion seen in this group of sharks ( E. blochii: up to ~50% of TL (Compagno, 1984)), lateral placement of the eyes has been hypothesized to result in a large blind area directly in fr ont of the cephalofoil (Walls, 1 942). However, the anterior

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33 position of the eyes on the distal tip of th e cephalofoil actually results in enhanced binocular overlap in E. blochii as compared to C. acronotus S. lewini and S. tiburo Sphyrna lewini was also found to have a greater binocular overlap than either S. tiburo or C. acronotus (McComb et al., 2009). Furthermor e, head yaw during swimming, which reduces the blind area in front of the head, was found to be greater in S. lewini and S. tiburo compared to C. acronotus (McComb et al., 2009). Stal k-eyed flies (Diopsidae) also display laterally displaced eyes and are conferred with improved binocular vision (Burkhardt and de la Motte, 1983). While vi sion is important for prey detection and tracking, it is unclear what c ontribution vision makes during the final stages of attack when the blind area becomes a liability. It is likely that other senses contribute to prey location in the absence of visual information when prey are close to the mouth (Gardiner and Atema, 2007). Through sphyrnid evolution, it is possible that anterior placement of the eyes in E. blochii and S. lewini was driven by selective pressures to reduce the blind area in these sphyrnid sharks. The positions of the incurrent and excurrent openings to the nasal capsule are also variable among species (re d lines, Figures 1.3 1.9). In the more basal E. blochii the nares are placed in a more medial positi on along the cephalofoil compared to more derived sphyrnids (Figure 1.4 vs. Figures 1.5 1 .9). It has been prev iously demonstrated that lateral placement of the nares, along with the evolution of the prenarial groove, has resulted in increased ability to resolve odors on opposite sides of the head (Kajiura et al., 2005). The length of the prenarial gr oove varies among sp ecies (Compagno, 1984; 1988). The distance between the two incurrent nares is signific antly greater in hammerhead sharks than outgroup car charhinids. Within sphyrnids, E. blochii has the

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34 greatest separation between incurrent nares, followed by S. zygaena and then S. lewini The internarial distance (the distance between the medial margin of the prenarial groove in sphyrnid or incurrent nares in carcharh inid shark) was significantly larger in S. lewini than both E. blochii and C. plumbeus, while the latter two species were not different from each other. These morphological differences in sphyrnid sharks create an olfactory system that samples a larger volume of water than comparably sized carcharhinid sharks (Kajiura et al., 2005). Recent work suggest s that the laterally placed nares of hammerhead sharks may confer an advantag e in detecting timing differences of odor arrival on opposite sides of the head. This is especially important for odor patch detection and patch following using klinotax is (Gardiner and Atema, 2010). While these studies support parts of the enhanced olfaction hypothe sis, the hypothesi zed increased olfactory acuity has not yet been fully invest igated. However, hammerhead sharks have been shown to have greater sensitivity to single amino acids presented at the incurrent nares (Tricas et al., 2009). In order to trul y resolve the olfactory abilities of sphyrnid sharks and test the enhanced olfactory hypothe sis further, a series of electrophysiological and behavioral experiments are needed to i nvestigate the responses to combinations of amino acids (Tricas et al., 2009; Meredith and Kajiura, In Press). Whereas eye and nares position show considerable variation through phylogeny, mouth position remains relative ly constant (blue lines, Figures 1.3 1.9). The cephalofoil expands and contracts around the relatively stat ic feeding structures. Mouth position may experience selective pressures to remain static based on the feeding mechanism’s role in prey capture and processing. Phylogenetic in ertia could also affect mouth position, in that mouth position will remain stationary without sufficient selective pressure for

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35 change. Furthermore, even in the presence of selective regimes that favor reorganization of the feeding elements, changes cannot oc cur without concomitant changes in other surrounding cranial structures to accommodate skeletal reorganization (Sakamoto et al., 2010). The electrosensory system has long been purported as the selective pressure driving evolution of the cephalofoil (Gilb ert, 1967; Compagno, 1984; 1988; Kajiura, 2001; Kajiura and Holland, 2002). Contrary to previous studies, the number of electrosensory pores on the ventral surface was not greater than that of the dorsal surface for all but three species ( C. acronotus S. mokarran and S. lewini ) (Table 1.3) (Gilbert, 1967; Kajiura, 2001; Cornett, 2006). Having a larger number of ventral pores could increase the spatial resolution of the electrosensory system and allow for more precise prey location when searchi ng at or near the bottom (Compagno, 1984; Kajiura, 2001; Kajiura and Holland, 2002). However, the species in this study found to have a significantly greater number of electros ensory pores on the ventral surface ( C. acronotus S. mokarran and S. lewini ) are not bottom associated but coastal-pelagic species that spend much of their time in the water colu mn (Compagno, 1984). It is possible that the increased number of ventrally located electroreceptors in th ese sphyrnid species allows for enhanced prey localization in the water co lumn. It should also be noted that ontogeny may play a role, as juvenile S. lewini do inhabit shallow water an d feed near the bottom (Compagno, 1984; 1988). Sphyrna lewini has a larger ventral bl ind area than the lemon shark, Negaprion brevirostris but does not differ significantly from C. acronotus or S. tiburo (McComb et al., 2009). Increased numbers of pores on the ve ntral surface may compensate for this ventrally located visual blind area.

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36 The overall distribution of el ectrosensory pores in hammer head sharks is similar among species on both the dorsal and ventral side s of the head and located within clearly demarcated pore fields (Figure 1.11) (Gilb ert, 1967; Kajiura, 2001). The pore maps reported here are consistent wi th those of previous studies, as is the average number of pores (Kajiura, 2001; Cornett, 2006). However, E. blochii lacks many of the pores along the anterior edge of the cephalofoil that ar e present in other hammerhead species (Figure 1.11). The reason for this difference is unkn own, but is most likely related to the placement of the nares. In E. blochii the nares are medially placed as compared to the lateral placement of the more derived sphyrnids resulting in a medial rather than lateral position for the anterior lateral pore fiel d (Gilbert, 1967) (Fig ures 1.1, 1.5, and 1.11). Lateral expansion of the cephalofoil and the resulting greater area of electroreceptor sampling equates to a larger s earch area for sphyrnid sharks compared to similar sized carcharhinid species (K ajiura and Holland, 2002). Juvenile S. lewini have comparable behavioral detection thresholds to similarly sized C. plumbeus (< 1 nV cm-1) and similar orientation distances to prey simulating electrodes (~30 cm) (Kajiura and Holland, 2002). To date, sampling area and det ection thresholds have been quantified for only two sphyrnid species ( S. lewini and S. tiburo ), neither of which possess the extreme lateral expansion seen in E. blochii (Compagno, 1984). When including other sphyrnid species with different degrees of lateral e xpansion, there would be differences expected among sphyrnid sharks in both sampling area an d distance prey can be detected from the midline of the body with greater lateral expa nsion resulting in larger sampling area and greater prey detection di stance (Kajiura, 2001 ; Kajiura and Holland, 2002). Having electrosensory pores spaced laterally on the head, without lateral movement of the

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37 ampullae themselves, could result in longer am pullary tubules and gr eater sensitivity to uniform electric fields compared to less la terally expanded sharks (Murray, 1974; Bennett and Clusin, 1978; Chu and Wen, 1979). The physiological threshol d for detection of electric fields and the behavior al threshold for reaction to elec tric fields have not yet been separated and could add further evidence to the enhanced electroreception hypothesis (Kajiura and Holland, 2002). Any description of the sens ory systems of an elasmobranch fish is incomplete without mention of the anterior cephalic mech anosensory lateral line. The lateral line plays a vital role in prey detection and tracking behavior (Gardiner and Atema, 2007). However, the anterior lateral line has onl y been described for a single species of sphyrnid, S. tiburo (Maruska, 2001). While this study di d not examine the anterior lateral line of other sphyrnids, the an terior lateral line canals ar e laterally displaced on the cephalofoil similar to the electrosensory sy stem (K.R. Mara, persona l observation). The consequences of lateral expansion on the la teral line system of sphyrnids remain enigmatic and should be the focus of a future study. Internal Cranial Volumes Correlation analyses of bot h non-phylogenetically corr ected and phylogenetically corrected data sets show that the internal volumes display a strong phylogenetic signal (differences between non-phylogenetically corr ected and phylogenetically corrected data sets) (Table 1.2 and Table 1.5 respectively) Although, the volumes of the various components in the head (hyomandibula, ce ratohyal, basihyal, Meckel’s cartilage, palatoquadrate cartilage, principal jaw closing muscles, eye, internal nasal capsule, internal olfactory tract, and internal braincase) remain relatively consistent through

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38 phylogeny, the orientation and spatial arrange ment does change. The morphometric and volumetric analyses indicate that the nasal capsule and optic cartilages are variable through phylogeny. This varia tion reflects the differing posi tion of the nares and eyes through phylogeny (Figures 1.4 – 1.9). The developmental and evolutionary pro cesses that govern the formation of the cephalofoil are not yet well unde rstood. However, the struct ure and development of the vertebrate head is partially determined by Hox genes along with pr eoptic and postoptic neural-crest derived ectomesenchyme (Gans and Northcutt, 1983; Gans, 1993; Manzanares et al., 2000; Kurata ni, 2005). There is also a po ssibility that hammerhead sharks with less laterally expanded cephalofoils arose as a result of changes in development, such as progenesi s or neoteny (Lim et al., 2010) Furthermore, the growth rate and organization of cartilaginous elemen ts can be influenced by environmental and developmental factors. Partic ularly, the growth of the brain can influence the shape of the braincase (Mller and Wagner, 1991; Herring, 1993). Sphyrnids have hypertrophied telence phalons occupying up to 67% of overall brain mass (Yopak et al., 2007). In sphyrnids, the proportion of the br ain occupied by the expanded olfactory bulb is quite large when compared to outgroup carcharhinids (7% vs. 3%) (Northcutt, 1977). Given the relatively co nsistent shape of the central core of the chondrocranium among sphyrnid an d carcharhinid species (Figur e 1.12), it is likely that brain organization and developmen t play a significant role in th e shape of the central core of the chondrocranium. It is unlikely that th e lateral wings of the cephalofoil are affected by changes in brain size as only the nasal capsules occupy the lateral cephalofoil.

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39 Constructional Constrai nts within the Cranium This study found few constructional constr aints within the head of hammerhead sharks (Table 1.2). Morphological constrai nts are of particular importance when investigating the form-functi on relationship among various co mponents within the head (Barel et al., 1989). Morphol ogical constraints often resu lt in one structure imposing constructional or architectural limitations on one or more surrounding structures (Barel, 1983; 1984; 1993; Barel et al., 1989; Motta and Kotrschal, 1992). Hypertrophy of the feeding apparatus may result in trade-offs between muscle or skeletal morphology (Barel, 1983; Devaere et al., 2001) and eye size, eye position, and overall head shape (Barel, 1993) in clariid catfishes and cichlid fishes. Constraint s are imposed on the feeding apparatus, by increases in eye si ze (Barel et al., 1989) and extrinsic eye musculature (von Scheven et al., 2006) in cichlid fishes and chick embryos respectively. Sensory structures have also been shown to negatively affect the development of neural structures such as the telencephalon (Str iedter and Northcutt, 2006). However, constructional constraints are not limited to sensory and fe eding structures (Nijhout and Emlen, 1998; Emlen, 2001). Traditionally, cons traints are defined as changes in one structure that result in functional or morphological tr ade-offs in a second, typically adjoining, structure (Barel, 1983; 1993; Barel et al., 1989; Nijhout and Emlen, 1998; Emlen, 2001). This definition has since been expanded to include trade-offs between or among structures that share a common de velopmental resource but may not be physically adjoining (Moczek and Nijhout, 2004). For the purposes of this study, constraints are defined as trade-offs be tween or among closely spaced structures.

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40 The vertebrate cranium is a complex sy stem that must c ontain structures associated with feeding, respiration, ne ural integration, sensory reception, and musculoskeletal support (Kohls dorf et al., 2008). The cepha lofoil of sphyrnid sharks also presents a system where the currently ac cepted explanation for its evolution relates to enhanced sensory percepti on, either electrosensory or olfactory (Tester, 1963a; Johnsen and Teeter, 1985; Kajiura, 2001; Ka jiura and Holland, 2002; Kajiura et al., 2005). Given the range of head expansion seen within sphyrnids, th ey present a system in which the constraints, if any, between or among sensory, neural, and feeding structures can be elucidated. No single el ement imposed significant constraints on the remaining elements. The few negative correl ations that were found dealt with the nasal capsule volume being negatively correlated with braincase, basi hyal, chondrocranial, and total volumes (red text, Table 1.2). As the volumes of the braincase, basihyal, chondrocranium, and total volume increased the volumes of the nasal capsule decreases. The negative correlations between nasal ca psule and braincase, chondrocranium, and total volume can be explained by space utilization of these adjacent structures. Given a finite amount of space within the chondrocra nium and consistent cranial volume among the hammerhead sharks (Tables 1.2 and 1.4) (K ajiura 2001), if one st ructure increases in volume, at least one of the remaining near by structures must show a concomitant decrease in volume. The explanation for th e remaining negative correlations with nasal capsule volume remains enigmatic and thes e correlations may not reflect any true constraint among these structur es. The only other negative correlation this analysis revealed was between head width and eye vol ume, where increased width of the head resulted in decreased volume of the eye. This is the result of the dorso-ventral flattening

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41 that occurs as head width increases among the species. The most extreme case is seen in E. blochii where the species with the greatest degr ee of lateral expansion also possesses the smallest eyes (Figures 1.4 and 1.12). As the cephalofoil is expande d laterally in basal species of sphyrnids, the depth, length, or both available for the skeletal structures surrounding the eyes and the eyes themselves is necessarily decreased. Thus, increasing lateral expansion, and the resulting dorso-ventr al flattening, constrai ns the volume of the eye. Musculoskeletal elements affecting eye size have been previ ously demonstrated in other fishes (see above and Barel, 1983; 1984; Huber, 2006). However, the manner in which expansion of the cephalofoil creates constraints on the eye is unique to sphyrnid sharks as few other vertebrates or invertebrates have lateral expansions of their head as extreme as those seen in hammerhead sharks. Feeding variables were positively correlated among species (blue text, Table 1.2). As the volume of the feeding muscles (Q MV, QMD, POV, and POD) increased, the volume of the palatoquadrate and Meckel’s ca rtilages, along with the hyomandibula, also increased. These positive correlations suggest that the four principal jaw closing muscles do not compete for space within the head, nor do the jaws or suspensory cartilages. The lack of negative correlations related to the f eeding structures indica tes that not only do they not compete for space among each other; they also do not cause constraints on other elements within the head because none of th e adjacent structures systematically decrease in volume. The various adductor mandibulae muscles of Lake Malawi cichlid fishes were also found to be positively correlated with each other (Hulsey et al., 2007). The strong positive correlation f ound among the jaw closing musc les can be explained by their common function among fishes. The positi ve correlations between the volumes of

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42 the palatoquadrate, Meckel’s cartilage, and hyomandibula can also be explained by their common biological role in jaw suspension and feeding (Huber, 2006). It is possible that there are constructional constr aints within the cephalofoil am ong elements that were not quantified in this study (e.g. connective ti ssue, peripheral ner vous system tissue, ampullary tubules, and respirat ory structures). For exampl e, a consequence of lateral cephalofoil expansion is the lateral displ acement of the electrosensory pores, which results in longer ampullary t ubules within the head. While longer tubules may confer a greater sensitivity (Murray, 1974; Bennett and Clusin, 1978; C hu and Wen, 1979), they also result in a greater volume within the cranium being taken up by the tubules leaving less volume for remaining elements. The Ancestral Sphyrnid Recent phylogenetic analyses indicate that the family Sphyrnidae is a monophyletic group within the family Carc harhinidae (Compagno, 1988; Naylor, 1992; Martin, 1995). There are two ge nera within the Sphyrnidae, Eusphyra and Sphyrna and eight currently recognized species along with some possible geminate species (Martin, 1993; Duncan et al., 2006; Quattro et al., 2006; Lim et al., 2010). The most recent phylogenetic analysis of the family (Lim et al., 2010) indicates that the evolution of the cephalofoil is not as simple as was once thought (Compagno, 1988). Instead, the cephalofoil underwent divergent evolution re sulting in two sepa rate evolutionary lineages, one leading to cephalofoil expansion ( Eusphyra lineage) and the second leading to cephalofoil contraction ( S. tiburo lineage). Furthermore, body size does not separate species into monophyletic groups (Lim et al., 2010). Ancestral character state reconstructions indicate that the ancestral sphyrnid shark was ~178 cm TL, putting it

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43 intermediate between large and small bodied extant ha mmerhead sharks (Table 1.6; Figure 1.1 Node 3). This shark was similar to extant large bodied sharks in extent of lateral head expansion, ~27% of TL. Other attempts at modeling body size for ancestral sphyrnid sharks have also revealed that th e evolution from a large bodied shark toward smaller bodied sharks is much more plausible than the reverse (Lim et al., 2010). Further supporting these data is the first occurrence of fossilized sphyrnid te eth belonging to the large bodied S. zygaena (Cappetta, 1987). Ancestral state reconstructi ons also show that the volumes of the internal elements also displayed trends through evolu tionary history. In general, the volume of the Meckel’s cartilage was greater than the volume of the palatoquadrate. This may be related to the Meckel’s cartilage having a la rger area of muscle attachment than the palatoquadrate cartilage (Wilga and Motta, 2000). This analysis also found that the volumes of the QMV and the POV were greater than the remaining jaw closing muscles through evolutionary history (Table 1.6) This matches data gathered for S. tiburo where masses of the QMV and the POV were greater than the remaining muscles (Mara et al., 2010). Evolution of the Cephalofoil There have been numerous hypothesis put forth regarding the evolution of the hammerhead shark cephalofoil. The hydr odynamic lift hypothesis states that the cephalofoil on the anterior end of the body pr ovides lift and increas es maneuverability (Nakaya, 1995; Driver, 1997) and the cephalofoil has some camber which may result in lift generation (Kajiura et al ., 2003). Furthermore, the p ectoral fins of hammerhead species with larger lateral expansions of the cephalofoil are proportionally smaller with

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44 total area of the cephalofoil and pectoral fins remaining constant across phylogeny (Thomson and Simanek, 1977; Compagno, 1984). Sphyrnid sharks were also found to be more maneuverable than similarly sized carcharhinid species. However, the cephalofoil was not found to act as a wi ng during turns. Instead the cephalofoil was kept relatively parallel to the substrat e (Kajiura et al., 2003). Various sensory based hypotheses have b een proposed regarding the evolution of the cephalofoil. The greater olfactory grad ient resolution hypothesis has received some support with the cephalofoil providing a greate r sampling area and enhanced klinotactic ability (Kajiura et al., 2005; Gardiner and Atema, 2010). Furtherm ore, sphyrnid sharks have been shown to have slightly greater se nsitivity to single amino acids (Tricas et al., 2009). However, olfactory epithelial su rface area does not differ among sphyrnid and carcharhinid species (Kajiura et al., 2005). The hammerhead cephalofoil results in the eyes being laterally displaced on the hea d. The enhanced binocular vision hypothesis proposes that the lateral placement of the eyes results in greater binocular overlap and increased visual field. Recent work has supported this hypothesis showing that the laterally positioned eyes do result in an increased binocular overlap in basal sphyrnid species compared to derived sphyrnid and carcharhinid species (McComb et al., 2009). The hypothesis that has received the most support is the enhanced electroreception hypothesis. The cephalofoil confers a greater sampling area for elect roreceptors and may provide a greater sensitivity to uniform electric fields (K ajiura, 2001; 2003; Kajiura and Holland, 2002). While other sensory modalitie s are important in prey tracking and localization, electroreception likely overrid es these other modalities during the final stages of attack (Kalmijn, 1971; Kimber et al., 2009). Fu rthermore, having laterally

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45 placed electroreceptors allows sphyrnid sharks to detect prey at a much greater distance from the mid-line of the body that similar sized carcharhinid species (Kajiura and Holland, 2002). Finally, the cephalofoil has also been hypothesized to function in prey manipulation (Strong et al., 1990 ; Chapman and Gruber, 2002) with the cephalofoil being used to stun and restrain prey against the seafloor. However, the data presented here show that other than a possible function in prey restraint, the feeding mechanism of sphyrnid sharks is not markedly differe nt from that of carcharhinid sharks. The data presented in this work along with the data of others (Tester, 1963a; b; Johnsen and Teeter, 1985; Kajiura, 2001; Kajiu ra et al., 2003; 2005; McComb et al., 2009) indicates that sensory systems appear to have been the major evolutionary force shaping the sphyrnid cephalofoil with few cha nges to the feeding structures. This study found little support for a feeding base d hypothesis beyond prey manipulation. Despite the sensory advantages conferre d by the cephalofoil, there are potential disadvantages associated with this laterally expanded structure. While the placement of the eyes on the lateral wings enhances bi nocular overlap and decreases the binocular convergence distance, the absolute size of the blind area in front of the cephalofoil is increased (McComb et al., 2009). Similarly, while the cephalofoil may provide sphyrnid sharks with increased maneuvera bility, it does so at the cost of turning ability. Sphyrnid sharks are not able to roll as much as simila rly sized carcharhinid species due to the risk of hitting the substrate with th e cephalofoil (Kajiura et al., 2003). Finally, the risk of predation, particularly upon the lateral wings of the cephalofoil, may be increased due to increased width of the head.

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46 CONCLUSIONS Hammerhead sharks display a diversity of cr anial shapes that vary with respect to the position of the eyes and nares, with little change in the relative po sition of the mouth. The eyes are first positioned at the anterior ed ge of the cephalofoil in basal species. Through phylogeny, eye position shifted to a more posterior position on the distal tip of the cephalofoil. External nares position is also variab le through sphyrnid phylogeny. Initially, in E. blochii, nares position is medial, similar to outgroup carcharhinids; through phylogeny, nares position shifted la terally, resulting in displ acement of the incurrent and excurrent narial openings. Mouth position, however, remains relatively static through phylogeny with minor changes in position and shape. The electrosensory system of sphyrnids is believed to have driven the evolution of the cephalofoil. This analysis revealed that electrosensory pore number is relatively conserved through sphyrnid phylogeny, and that overall distribution of electroreceptive pores is similar among all species except E. blochii This study also demonstrated that, within the cephalofoil, many of the elements do not impose constructio nal constraints upon each other. The few constraints that do occur are confined to th e volume of the nasal capsule and eye. Nasal capsule volume was negatively correlated w ith braincase and to tal chondrocranial volume, and eye size is inversely related with head width. Consequently, as head width increases, there is a concomitant decrease in eye volume. Not only were most elements not constrained, the feeding muscles and th e cartilages they rest upon showed positive correlations through phylogeny. This indicates th at the feeding elements do not constrain other elements and are free to change in volume within the head.

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47 LITERATURE CITED Adams, D. C. and Rohlf, F. J. (2000). Ecological character displacement in Plethodon : biomechanical differences found from a geometric morphometric study. Proceedings of the National Academy of Sc iences of the United States of America 97 4106-4111. Aldrich, J. (1995). Correlations genuine and spurious in Pearson and Yule. Statistical Science 10 364-376. Barel, C. D. N. (1983). Towards a constructiona l morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology 33 357-424. Barel, C. D. N. (1984). Form-relations in the contex t of constructional morphology: the eye and suspensorium of lacustrine Ci chlidae (Pisces, Teleostei): with a discussion on the implications for phyloge netic and allometric form-interactions. Netherlands Journal of Zoology 34 439-502. Barel, C. D. N. (1993). Concepts of an architect onic approach to transformation morphology. Acta Biotheoretica 41 345-381. Barel, C. D. N., Anker, C. C., Witte, F., Hoogerhoud, R. J. C., and Goldschmidt, T. (1989). Constructional constraint a nd its ecomorphological implications. Acta Morphologica Neerlando-Scandinavica 27 83-109. Bennett, M. V. L. and Clusin, W. T. (1978). Physiology of the ampulla of Lorenzini, the electroreceptor of elasmobranchs. In Sensory Biology of Sharks, Skates, and Rays Eds. E. S. Hodgson and R. F. Mathewson, pp. 483-505. Arlington, Virginia: Office of Naval Research. Bock, W. J. (1980). The definition and rec ognition of biological adaptation. American Zoologist 20 217-227. Bock, W. J. and von Wahlert, G. (1965). Adaptation and the form-function complex. Evolution 19 269-299. Bookstein, F. L. (1991). Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge: Cambridge University Press. Bookstein, F. L. (1996a). Combining the tools of geometric morphometrics. In Advances in Morphometrics Eds. L. F. Marcus M. Corti A. Loy G. J. P. Naylor and D. Slice, pp. 131-151. New York: Plenum.

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48 Bookstein, F. L. (1996b). Standard formula for the uniform shape component in landmark data. In Advances in Morphometrics Eds. L. F. Marcus M. Corti A. Loy G. J. P. Naylor and D. Slice, pp. 153-168. New York: Plenum Press. Burkhardt, D. and de la Motte, I. (1983). How stalk-eyed flie s eye stalk-eyed flies: observations and measurements of the eyes of Cyrtodiopsis whitei (Diopsidae, Diptera). Journal of Comparative Physiology A 151 407-421. Cappetta, H. (1987). Chondrichthyes II. Mesozoic and Cenozoic Elasmobranchii. Stuttgart: Fischer. Cavalcanti, M. J. (2004). Geometric morphometric anal ysis of head shape variation in four species of hammerhead sharks (Carcharhiniformes: Sphyrnidae). In Morphometrics Applications in Biology and Paleontology Ed. A. M. T. Elewa, pp. 97-113. Berlin: Springer-Verlag. Chapman, D. D. and Gruber, S. H. (2002). A further observation of the prey-handling behavior of the great hammerhead shark, Sphyrna mokarran : predation upon the spotted eagle ray, Aetobatus narinari Bulletin of Marine Science 70 947-952. Chu, Y. T. and Wen, M. C. (1979). Monograph of fishes of China (No. 2): a study of the lateral-line canal system and that of Lorenzini ampulla and tubules of elasmobranchiate fishes of China. Shanghai: Science and Technology Press. Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shar k species known to data. Part 2. Carcharhiniformes. FAO Fish. Synop.: (125) Vol. 4, Pt. 2. Compagno, L. J. V. (1988). Sharks of the Order Carcharhiniformes. Princeton: Princeton University Press. Cornett, A. D. (2006). Ecomorphology of shark elec troreceptors, pp. 102. MS Thesis. Florida Atlantic University, Boca Raton, FL. Devaere, S., Adriaens, D., Verraes, W., and Teugels, G. G. (2001). Cranial morphology of the anguilliform clariid Channallabes apus (Gnther, 1873) (Teleostei: Siluriformes): are adap tations related to powerful biting? Journal of Zoology, London 255 235-250. Devaere, S., Adriaens, D., Teugels, G. G., and Verraes, W. (2005). Morphology and spatial constraints in a dorso-ventrally flattened skull, with a revised species description of Platyallabes tihoni (Poll, 1944). Journal of Natural History 39 1653-1673.

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49 Driver, K. H. (1997). Hydrodynamic properties and ecomorphology of the hammerhead shark (Family Sphyrnidae) cephalofoil ., pp. 159. Dissertation. University of California Davis, Davis, CA. Dullemeijer, P. (1958). The mutual structural influen ces of the elements in a pattern. Archives Nerlandaises de Zoologie 13 174-188. Dullemeijer, P. (1974). Concepts and approaches in animal morphology. Assen: The Netherlands: Van Gorcum. Duncan, K. M., Martin, A. P., Bowen, B. W., and De Couet, H. G. (2006). Global phylogeography of the scalloped hamme rhead shark (Sphyrna lewini). Molecular Ecology 15 2239-2251. Emlen, D. J. (2001). Costs and the diversification of exaggerated animal structures. Science 291 1534-1536. Felsenstein, J. (1985). Phylogenies a nd the comparative method. American Naturalist 125 1-15. Gans, C. (1993). Evolutionary origin of the vertebrate skull. In The Skull vol. 2 Eds. J. Hanken and B. K. Hall, pp. 1-35. Chicago: University of Chicago Press. Gans, C. and Northcutt, R. G. (1983). Neural crest and the or igin of vertebrates: a new head. Science 220 268-274. Garland Jr., T., Bennett, A. F., and Rezende, E. L. (2005). Phylogenetic approaches in comparative physiology. Journal of Expe rimental Biology 208 3015-3035. Gardiner, J. M. and Atema, J. (2007). Sharks need the la teral line to locate odor sources: rheotaxis and eddy chemotaxis. Journal of Experimental Biology 210 1925-1934. Gardiner, J. M. and Atema, J. (2010). The function of b ilateral odor arrival time differences in olfactory orientation of sharks. Current Biology, doi:10.1016/ j.cub.2010.04.053. Gilbert, C. R. (1967). A revision of the hammerh ead sharks (Family Sphyrnidae). Proceedings of the United States National Museum 119 1-88. Haenni, E. G. (2001). On the growth, func tional morphology, and embryological development of the cephalofoil in the bonnethead shark, Sphyrna tiburo pp. 253. Dissertation. Clemson Un iversity, Clemson, SC.

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53 Quattro, J. M., Stoner, D. S., Driggers, W. B., Anderson, C. A., Priede, K. A., Hoppmann, E. C., Campbell, N. H., Duncan, K. M., and Grady, J. M. (2006). Genetic evidence of cryptic speciation within hammerhead sharks (genus Sphyrna ). Marine Biology 148 1143-1155. Reif, W. E., Thomas, R. D. K., and Fischer, M. S. (1985). Constructional morphology: the analysis of cons traints in evolution. Acta Biotheoretica 34 233-248. Sakamoto, M., Lloyd, G. T., and Benton, M. J. (2010). Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance. Journal of Evolutionary Biology 23 463-478. Schultze, H.-P. (1993). Patterns of dive rsity in the sk ulls of jawed fishes. In The Skull vol. 2 Eds. J. Hanken and B. K. Hall, pp. 189-254. Chicago: University of Chicago Press. Sheets, H. D. (2003). IMP Integrative Morphometrics Package. Buffalo, NY: Department of Physics, Canisius College. Striedter, G. F. and Northcutt, R. G. (2006). Head size constrains forebrain development and evolution in ray-finned fishes. Evolution & Development 8 215222. Strong Jr., W. R., Snelson, F. F., and Gruber, S. H. (1990). Hammerhead shark predation on stingrays: an obs ervation of prey handling by Sphyrna mokarran Copeia 1990 836-840. Tester, A. L. (1963a). The role of olf action in shark predation. Pacific Science 17 145170. Tester, A. L. (1963b). Olfaction, gestation and the co mmon chemical sense in sharks. In Sharks and Survival Ed. P. W. Gilbert, pp. 255-285. Boston: C.C. Heath and Company. Thomson, K. S. and Simanek, D. E. (1977). Body form and locomotion in sharks. American Zoologist 17 343-354. Trapani, J. (2003). Geometric morphometric anal ysis of body-form variability in Cichlasoma minckleyi the Cuatro Cienegas cichlid. Environmental Biology of Fishes 68 357-369. Tricas, T. C., Kajiura, S. M., and Summers, A. P. (2009). Response of the hammerhead shark olfactory epithelium to amino acid stimuli. Journal of Comparative Physiology A 195 947-954.

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54 von Scheven, G., Alvares, L. E., Mootoosamy, R. C., and Dietrich, S. (2006). Neural tube derived signals and Fgf8 act an tagonistically to specify eye versus mandibular arch muscles. Development 133 2731-2745. Walls, G. L. (1942). The Vertebrate Eye and its Adaptive Radiation. London: Hafner Publishing Company. Wilga, C. D. and Motta, P. J. (2000). Durophagy in sharks : feeding mechanics of the hammerhead Sphyrna tiburo Journal of Experimental Biology 203 2781-2796. Yopak, K. E., Lisney, T. J., Collin, S. P., and Montgomery, J. (2007). Variation in brain organization and cerebellar folia tion in chondrichthyans: sharks and holocephalans. Brain Behavior and Evolution 69 280-300.

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55 Figure 1.1. Phylogeny of the hammerhead shar ks modified from Lim et al. (2010). Based on the nuclear genes ITS2, Dlx1, and Dlx2 and the mitochondrial genes NADH dehydrogenase 2, cytochrome b cytochrome oxidase I, and D-loop. Differences in head shape among the species are indi cated with non scaled line dr awings of the cephalofoil. Body size differences are shown among the speci es with a generalized body shape scaled to maximum reported size for each species. Numbers above the nodes are posterior probabilities and numbers below the node are BE ST credibility values. Numbers to the right of the nodes indicate nodes for ancestral state reconstructions. Head shapes and body outlines modified from Compagno, 1984. Scale bar = 1 m.

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56 Figure 1.2. External landmarks chosen for geometric morphometrics. Landmarks were chosen to represent the position of the m outh (10, 11, 12), eye (3, 4), incurrent and excurrent nares (5, 6), and overall cephalofo il shape (1, 2, 7, 8, 9). Landmarks were digitized on the left side of the head only, and comparisons were anchored at landmarks one and nine.

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57 Figure 1.3. Shape differences between C. acronotus (gray) and R. terraenovae (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are il lustrated on the animal’s left side only. The head expands anteriorly (white vectors) along with the position of the nares (red) and eyes (yellow). The mouth is also ex panded and shifted anterolaterally in R. terraenovae

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58 Figure 1.4. Shape differences between C. acronotus (gray) and E. blochii (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are illustrated on the animal’s left side only. The cephalofoil expands laterall y and the eyes (yellow) and nares (red) move laterally with the expansion. Mouth position shifts slightly posteromedially.

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59 Figure 1.5. Shape differences between E. blochii (gray) and S. mokarran (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are illustrated on the animal’s left side only. Cephalofoil expansion decreases while eye pos ition shifts anteromedially. However, nares position shift anterior ly and mouth position shif ts slightly posteriorly.

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60 Figure 1.6. Shape differences between S. mokarran (gray) and S. zygaena (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are il lustrated on the animal’s left side only. Cephalofoil expansion increases slightly a nd the eyes (yellow) and nares (red) shift posterolaterally. Mouth position shifts slight ly anterior however no other major changes are seen

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61 Figure 1.7. Shape differences between S. zygaena (gray) and S. lewini (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are il lustrated on the animal’s left side only. Cephalofoil shape remains largely unchanged. However, eye (yellow) and nares position (red) shift anteriorly. Mouth position also remains unchanged.

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62 Figure 1.8. Shape differences between S. lewini (gray) and S. tudes (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are illustrated on the animal’s left side only. Cephalofoil expansion decreases laterally and increases rostrally while eye and nares position shift anteromedially. Mouth position remains unchanged.

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63 Figure 1.9. Shape differences between S. tudes (gray) and S. tiburo (green). Differences in shape are illustrated using vector transformations. Shape differences are assumed to be bilaterally symmetrical and are illustrated on th e animal’s left side only. Eye and nares position is shifted medially while the cephalofo il decreases in lateral expansion. Mouth position, however, remains unchanged.

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64 Figure 1.10. Principal components analysis of head shape within carcharhinid and sphyrnid sharks. PC 1 explained 78.8% of th e variation and indicat es decreasing lateral expansion of the cephalofoil. PC 2 explai ned 13.5% of the variation and represents lateral placement of the nares and anterior placement of the eyes.

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65 Figure 1.11. Electrosensory pore maps overlai n onto phylogeny. Left side of each map is the dorsal surface and the right side is the ventral surface of the head. Both S. lewini and C. acronotus had a greater number of ventral pores than R. terraenovae and S. tiburo (p < 0.001). Phylogeny simplified from Lim et al., 2010. Numb ers indicate nodes for ancestral state reconstructions.

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66 Figure 1.12. Representative reconstructions of the internal elements of the head of hammerhead sharks overlain onto phylogeny. The chondro cranium has been removed from half of the head to illustrate other el ements. Phylogeny simp lified from Lim et al., 2010. Numbers indicate nodes for ancestral state reconstructions Light green = chondrocranium, green = braincase, orange = olfactory tract, red = nasal capsule, yellow = eye, light blue = palatoquadrate, dark bl ue = Meckel’s cartilage, pink = hyomandibula, purple = ceratohyal, and dark green = basihyal. Scale bars = 5 cm

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67 Figure 1.13. Chondrocranial stru ctures of the cephalofoil of Eusphyra blochii Modeled after Compagno, 1988. FPP – distal wing of fuse d preorbital and postorbital processes, IOL – distal lobe of preorbital process, LJ – line of fusion of preorbital and postorbital processes, LR – lateral rostral cartilage, NC – nasal capsule, OW – anterior wing of nasal capsule, PR – preorbital process, PT – postorbital process, RW – rostral wing

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68 Table 1.1. Average volume (cm3) of the eye standard error measured using three different methods. Species In Animal Isolated Displacement Within Species Pooled Species R. terraenovae 5.34 0.21 6.03 0.38 6.33 0.33 0.13 0.464 E. blochii 1.79 0.14 2.1 0.17 2.1 0.21 0.41 S. lewini 28.41 0.63 31.73 0.78 31.33 1.2 0.08 S. tiburo 1.84 0.18 2.13 0.03 2 0 0.23 Eye volume was measured from CT scans of th ree individuals with the eyes intact (In Animal), from CT scans of the eyes after removal from the animal (Isolated), and via water displacement (Displacement). The diffe rent methods for measuring eye volume were not different within species ( S. tiburo p = 0.23, S. lewini p=0.08, E. blochii p=0.41, R. terraenovae p=0.13) or when species are pooled (p=0.46).

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69 Table 1.2. Correlation matrix performed on phyl ogenetically corrected data for sphyrnid and outgroup carcharhinid species. Head Width QMV QMD POV POD Eye Nasal Capsule Olfactory Tract Braincase Head Width 1.000-.423-.530-.273-.377 -.910 -.621.250 .650 .202.140.300.231 .006 .094.316 .081 QMV (cm3) 1.000 .962.898.846 .497.628.612 -.055 . .001.008.017 .158.091.098 .459 QMD (cm3) . 1.000 .917.901 .654 .740 .628 -.184 . .005.007 .079 .046 .091 .363 POV (cm3) . 1.000 .962 .392.605 .838 .027 . . .001 .221.101 .019 .480 POD (cm3) . . 1.000.447 .777.760 -.227 . . .187 .035.040 .333 Eye (cm3) . . 1.000.618-.020 -.500 . . . .095.485 .156 Nasal Capsule (cm3) . . . 1.000.311 -.762 . . . .274 .039 Olfactory Tract (cm3) . . . 1.000 .327 . . . . .264 Braincase (cm3) . . . . 1.000 . . . . Palatoquadrate (cm3) . . . . . . . . . Meckel’s cartilage (cm3) . . . . . . . . . Hyomandibula (cm3) . . . . . . . . . Ceratohyal (cm3) . . . . . . . . . Basihyal (cm3) . . . . . . . . . Chondrocranium (cm3) . . . . . . . . . Total Volume (cm3) . . . . . . . . . Dorsal Pore Count (#) . . . . . . . . . Ventral Pore Count (#) . . . . The top line within a structure is the corre lation coefficient and the bottom line is the pvalue. Blue = a positive correlation betw een the two structures. Red = a negative correlation between the two structures.

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70 Table 1.2 Continued. Correlation matrix pe rformed on phylogenetical ly corrected data for sphyrnid and outgroup carcharhinid species. Palatoquadrate Meckel’s cartilage Hyomandibula Ceratohyal Basihyal Chondrocranium Total Volume Dorsal Pore Count Ventral Pore Count Head Width -.459-.393-.298-.524.657 .829 .621 .762 .414 .180.221.283.143.078 .021 .094 .039 .207 QMV (cm3) .943.958.951.811 -.198-.241-.107 -.316 .100 .002.001.002.025 .354.323.420 .271 .426 QMD (cm3) .991.984.957.852 -.322-.385-.237 -.270 .142 .000.000.001.016 .267.226.326 .302 .394 POV (cm3) .949.964.984 .633-.179-.179-.055 -.075 .242 .002.001.000 .089.367.367.459 .444 .322 POD (cm3) .923.919.945 .554-.431-.403-.312 -.187 .045 .004.005.002 .127.197.214.274 .362 .466 Eye (cm3) .615.545.426 .744 -.497-.696-.478 -.451 -.037 .097.132.200 .045 .158.062.169 .184 .472 Nasal Capsule (cm3) .705.656.649.493 -.850-.823-.810 -.446 -.348 .059.078.081.160 .016.022.025 .188 .250 Olfactory Tract (cm3) .712 .748.803 .378.138.218.230 .439 .563 .056 .044.027 .230.397.339.330 .192 .122 Braincase (cm3) -.114-.039-.014-.053 .967.948.994 .598 .714 .415.471.489.460 .001.002.000 .105 .055 Palatoquadrate (cm3) 1.000 .995.974.826 -.267-.322-.174 -.166 .234 .000.001.021 .305.267.371 .377 .328 Meckel’s cartilage (cm3) 1.000 .988.811 -.199-.244-.102 -.139 .259 . .000.025 .353.321.424 .397 .310 Hyomandibula (cm3) . 1.000.723-.196-.201-.090 -.114 .225 . .052.355.352.433 .415 .334 Ceratohyal (cm3) . 1.000-.073-.227-.057 -.153 .344 . . .446.332.457 .386 .252 Basihyal (cm3) . . 1.000 .960.985 .616 .703 . . .001.000 .096 .060 Chondrocranium (cm3) . . 1.000 .946 .690 .630 . . . .002 .065 .090 Total Volume (cm3) . . . 1.000 .572 .698 . . . .118 .061 Dorsal Pore Count (#) . . . 1.000 .784 . . . . .033 The top line within a structure is the corre lation coefficient and the bottom line is the pvalue. Blue = a positive correlation while red = a negative correlation.

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71 Table 1.3. Average electrosensory pore coun ts standard erro r for both dorsal and ventral surfaces of the head. Species Number of Dorsal Po res Number of Ventral Pores C. acronotus 898.8 22.15 1468.4 42.85 R. terraenovae 962.4 65.88 896.4 25.92 E. blochii 1270 29.24 1254 15.28 S. mokarran 917.6 30.54 ** 1300 30.57 ** S. zygaena 889 41 1103 5 S. lewini 1303.2 113.75 *** 1634 140.10 *** S. tudes 1254.8 41.48 1344.8 38.71 S. tiburo 904.8 21.49 1034 12.88 The number of both dorsal a nd ventral electrose nsory pores was not correlated with changes in any other struct ures within the head. C. acronotus S. mokarran and S. lewini have more pores on the ventral surface than the dorsal surface but all others are not different. *, **, *** p < 0.001. N = 5.

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72 Table 1.4. Average standard error for volumes for each intern al element of hammerhead shar ks and outgroup carcharhinids. Head Width TL QMV QMD 1&2 POV POD Eye Nasal Capsule Olfactory Tract Braincase C. acronotus 11.24 0.41 100.67 4.05 16.33 2.96 10.33 1.86 9.67 1.76 3.33 0.33 11.54 1.01 12.53 1.33 0 33.41 2.92 R. terraenovae 8.93 0.21 86.20 1.99 9.83 1.36 4.50 0.50 2.67 0.67 1.67 0.33 10.67 0.42 9.45 0.65 0 17.38 0.57 E. blochii 58.00 3.33 145.97 9.91 13.67 2.91 9.33 2.85 15.00 2.65 8.83 1.59 3.57 0.29 34 6.30 7.68 2.77 68.44 13.99 S. mokarran 54.43 3.31 234.67 12.39 112.67 17.37 58.67 11.85 82.67 11.62 50.00 8.08 24.85 1.25 92.83 20.33 35.99 2.98 285.62 42.85 S. zygaena 68.00 8.00 262.50 30.50 47.50 16.50 25.25 9.75 46.00 17.00 22.00 8.00 21.18 3.29 62.65 14.1 15.73 4.62 327.1 73.07 S. lewini 61.53 1.32 257.93 2.45 49.00 9.54 36.33 6.12 65.67 12.81 34.00 4.73 47.21 9.27 78.8 16.18 34.15 5.63 331.83 20.47 S. tudes 23.50 1.74 81.6 10.27 2.33 0.88 1.63 0.41 4.50 1.32 2.00 0.58 1.00 0.06 5.41 1.11 1.05 0.25 20.85 3.98 S. tiburo 14.00 0.37 90.83 2.09 4.00 0.00 3.50 0.29 7.00 0.58 4.17 0.44 3.67 0.35 11.91 0.97 0 20.55 1.82 Values in cm3 unless otherwise noted.

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73 Table 1.4 Continued. Average standard error for volumes fo r each internal element of ha mmerhead sharks and outgroup carcharhinids. Palatoquadrate Meckel’s cartilage Hyomandibula Ceratohyal Basihyal Chondrocranium Total Volume Dorsal Pore Count (#) Ventral Pore Count (#) C. acronotus 11.15 1.55 14.65 1.85 4.33 0.66 6.15 0.75 2.19 0.24 61.94 6.70 704.01 96.76 898.80 22.15 1468.40 42.85 R. terraenovae 5.19 0.18 7.05 0.71 1.97 0.10 2.43 0.15 1.17 0.13 31.8 1.83 372.66 33.01 962.40 65.88 896.40 25.92 E. blochii 11.43 2.00 15.5 3.15 6.71 1.12 4.77 0.45 1.91 0.09 161.07 22.47 1027.73 183.68 1270.00 29.24 1254.00 15.28 S. mokarran 73.57 11.61 101.43 17.18 34.69 6.26 20.35 2.98 7.06 1.06 512.17 81.21 5098.92 828.58 917.60 30.54 1300.00 30.57 S. zygaena 32.56 9.95 45.03 13.28 19.95 6.95 14.58 5.22 10.00 2.83 677.35 195.7 6040.19 1832.63 889.00 41.00 1103.00 5.00 S. lewini 55.32 11.25 69.86 12.43 26.06 6.95 19.88 3.95 10.04 1.61 571.17 27.42 6009.92 305.07 1303.20 113.75 1634.00 140.10 S. tudes 2.22 0.53 2.96 0.67 1.34 0.31 0.98 0.23 1.11 0.26 41.99 7.37 409.12 89.45 1254.80 41.48 1344.80 38.71 S. tiburo 4.45 0.34 5.49 0.45 2.18 0.10 1.59 0.03 0.61 0.07 24.53 1.77 315.95 15.98 904.80 21.49 1034.00 12.88 Values in cm3 unless otherwise noted .

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74 Table 1.5. Correlation matrix performed on raw size-removed data for sphyrnid and outgroup carcharhinid species. Head Width QMV QMD POV POD Eye Nasal Capsule Olfactory Tract Braincase Head Width 1.00 -.673-.686 .041.070 -.892 -.229 .441 .188 .000.000 .426.375 .000 .146 .018 .195 QMV (cm3) 1.000 .936 .242.237 .639.562 .028 .076 .000 .133.138 .001.003 .449 .364 QMD (cm3) 1.000 .452.404.694.628 .037 .176 .015.028.000.001 .433 .211 POV (cm3) 1.000 .822 -.008 .362 .236 .452 .000 .486 .045 .139 .015 POD (cm3) 1.000.028 .544.483 .311 .450 .004.010 .075 Eye (cm3) 1.000 .354 -.244 -.058 .049 .131 .396 Nasal Capsule (cm3) 1.000.298 -.181 .084 .205 Olfactory Tract (cm3) 1.000 .282 .096 Braincase (cm3) 1.000 . . . . Palatoquadrate (cm3) . . . . . . . . . Meckel’s cartilage (cm3) . . . . . . . . . Hyomandibula (cm3) . . . . . . . . . Ceratohyal (cm3) . . . . . . . . . Basihyal (cm3) . . . . . . . . . Chondrocranium (cm3) . . . . . . . . . Total Volume (cm3) . . . . . . . . . Dorsal Pore Count (#) . . . . . . . . . Ventral Pore Count (#) . . . . The top line within a structure is the corre lation coefficient and the bottom line is the pvalue. Blue = a positive correlation betw een the two structures. Red = a negative correlation between the two structures.

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75 Table 1.5 Continued. Correlation matrix performed on raw size-removed data for sphyrnid and outgroup carcharhinid species. Palatoquadrate Meckel’s cartilage Hyomandibula Ceratohyal Basihyal Chondrocranium Total Volume Dorsal Pore Count Ventral Pore Count Head Width -.639-.625-.374-.651 -.282 .469 -.148 .553 .098 .001.001.039.000 .096 .012 .250 .003 .328 QMV (cm3) .899.924.808.878 .329.000.313 -.485 -.044 .000.000.000.000 .062.499.073 .009 .422 QMD (cm3) .970.979.885.900 .281-.074.324 -.475 .115 .000.000.000.000 .097.369.066 .011 .300 POV (cm3) .464.456.638 .298-.074.020.248 -.147 .415 .013.014.001 .084.369.464.127 .252 .024 POD (cm3) .431.399.568 .154-.328-.177.011 -.148 .196 .020.030.002 .242.063.210.481 .250 .185 Eye (cm3) .701.676.443.682 .274 -.380 .155 -.392 -.015 .000.000.017.000 .103 .037 .240 .032 .472 Nasal Capsule (cm3) .650.633.696.465 -.420 -.338-.330 -.253 -.209 .000.001.000.013.023 .057.062 .122 .170 Olfactory Tract (cm3) .151.146.240-.118-.243.244.029 .445 .190 .246.253.135.296.132.131.448 .017 .192 Braincase (cm3) .204.226.326.190 .548.659.828 .043 .463 .175.150.064.193 .003.000.000 .423 .013 Palatoquadrate (cm3) 1.000 .989.918.899 .238-.059.305 -.416 .180 .000.000.000 .137.395.079 .024 .206 Meckel’s cartilage (cm3) 1.000 .912.899 .282-.002.349 -.413 .150 .000.000 .097.496.051 .025 .247 Hyomandibula (cm3) 1.000 .819 .145.076.314 -.388 .157 .000 .255.365.072 .034 .238 Ceratohyal (cm3) 1.000 .477 .101 .404 -.385 .237 .011 .323 .028 .035 .138 Basihyal (cm3) 1.000 .608.859 -.011 .381 .001.000 .480 .036 Chondrocranium (cm3) 1.000 .653 .272 .364 .000 .104 .044 Total Volume (cm3) 1.000 -.006 .432 .489 .020 Dorsal Pore Count (#) 1.000 .463 .013 The top line within a structure is the corre lation coefficient and the bottom line is the pvalue. Blue = a positive correlation while red = a negative correlation.

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76 Table 1.6. Ancestral state reconstructions at each of the nodes along sphyrnid phylogeny (Figure 1). Basal Derived Node 2 3 4 7 5 6 Head Width (cm) 38.36 47.45 46.84 50.89 38.87 24.29 TL (cm) 163.21177.49181.91199.54160.69 108.13 QMV Volume (cm3) 21.03 22.09 23.41 30.89 15.61 5.32 QMD Volume (cm3) 13.32 14.00 14.78 18.42 10.89 4.09 POV Volume (cm3) 21.74 25.15 26.81 32.74 21.01 8.88 POD Volume (cm3) 10.89 13.39 14.16 17.20 10.99 4.56 Eye Volume (cm3) 9.98 9.75 10.85 13.34 9.21 3.38 Nasal Capsule Volume (cm3) 32.01 37.72 38.51 45.62 29.12 12.66 Olfactory Tract Volume (cm3) 6.58 9.12 9.53 11.87 6.87 2.06 Braincase Volume (cm3) 101.38123.02132.48168.2198.43 36.64 Palatoquadrate Volume (cm3) 17.24 18.66 19.78 24.52 14.87 5.47 Meckel’s cartilage Volume (cm3) 23.00 24.94 26.43 33.08 19.49 7.09 Hyomandibula Volume (cm3) 8.88 10.10 10.63 13.27 7.77 2.94 Ceratohyal Volume (cm3) 7.10 7.30 7.65 9.38 5.73 2.16 Basihyal Volume (cm3) 3.48 3.79 4.09 5.05 3.22 1.36 Chondrocranium Volume (cm3) 194.64237.79250.30320.42174.21 60.37 Total Volume (cm3) 1790.892112.352302.972951.161726.37 639.62 Dorsal Pore Count (#) 1042.981070.191051.881005.431104.90 1085.22 Ventral Pore Count (#) 1286.991257.941257.251231.311306.94 1230.29 Indicates that at node 2, Figure 1.1, the most common ancestor between sphyrnid and carcharhinid sharks was a rela tively large bodied shark (163. 21 cm TL) that possessed a moderately expanded cephalofoil (~23% of TL). These values place the ancestral shark intermediate between large and small bodied ha mmerhead sharks in le ngth and similar to large bodied hammerhead sharks ( S. mokarran S. zygaena and S. lewini ) in degree of lateral head expansion (Compagno, 1984; 1988). Nodes are organized from basal on the left to more derived on the right.

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77 CHAPTER 2: FUNCTIONAL MORPHOLOGY OF THE FEEDING APPARATUS IN HAMMERHEAD SHARKS (SPHYRNIDAE): A PHYLOGENETIC PERSPECTIVE ABSTRACT Hammerhead sharks offer a unique opportun ity to study form and function through phylogeny. Because sphyrnid sharks posses cranial morphologies with extreme variation, they can be used to address questions a bout the evolution of cranial design and investigate the effects of changes in head morphology on feeding structures and ecologically relevant pe rformance parameters such as bite force. Adult individuals of Eusphyra blochii Sphyrna mokarran S. lewini S. tudes S. tiburo Carcharhinus acronotus and Rhizoprionodon terraenovae were chosen to represent a continuum of head shape through phylogeny. The cross sec tional areas of the four principal jaw adductors as well as the mechanical advantag e of the jaws were used to estimate the theoretical maximum bite force. Additiona lly, the volume of each muscle along with the volume the palatoquadrate a nd Meckel’s cartilage, and hyoi d arch were determined through reconstructed CT scans. Both an terior (18.2 – 642.22 N) and posterior (71.08 – 1839.43 N) absolute bite force exceeded a fu ll order of magnitude Within sphyrnid sharks anterior and posterior mechanical advantage ranged from 0.12 – 0.26 and 0.76 – 1.01 respectively with outgroup carcharhinids having slightly greater anterior and posterior mechanical advantages. These valu es of anterior mechanical advantage place sphyrnid sharks among other fishes classified as having low to intermediate jaw leverage

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78 systems. Multiple linear regression indicated that the best predictor of anterior bite force was the force produced by the preorbitalis ve ntral while posterior bite force was best predicted by the force produced by the preorbita lis ventral and preorb italis dorsal along with posterior mechanical advantage. Sizeremoved bite force analysis indicated that E. blochii S. zygaena and S. tiburo all produce less force than would be predicted based on their length. Negative correlations were al so found within the feeding structures. Particularly striking was the negative correlations between posterior bite force and the volumes of the POV, POD, palatoquadrate, Meckel’s cartilage, and hyomandibula. Despite these negative correlations, much of the feeding apparatus remains unchanged through evolutionary history indicating few constructiona l constraints within the cephalofoil. These results, al ong with previous data, lead to the conclusion that within sphyrnid sharks the feeding bauplan has been conserved with few changes to the feeding apparatus and biomechanics. Instead, change s to the cephalofoil are confined to the chondrocranial elements and sensory structures. INTRODUCTION Diversity in cranial morphology is often associated with the occupation of novel habitats due, in part, to occupation of diff erent feeding niches (Grant and Grant, 1995; Caldecutt and Adams, 1998; Herrel et al., 2001a ; b; Adriaens et al., 2009). Furthermore, chondrichthyan fishes occupy a diverse range of feeding niches due, in part, to divergent cranial morphologies (e.g. horn sharks (Summe rs et al., 2004; H uber et al., 2005) and cownose rays (Summers, 2000)). In an a ttempt to understand th is morphological and functional diversity, several studies have focused on the functional morphology of the

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79 feeding apparatus (reviewed in Motta, 2004). Most of these studies focus on a single species (Frazzetta and Prange, 1987; Shirai and Nakaya, 1992; Wu, 1994; Motta et al., 1997; Wilga and Motta, 1998a; b; Dean and Motta, 2004a; b; Matott et al., 2005), with notable exceptions (Summers, 2000). Such performance-based comparative studies provide a window into the e volution of vertebrate de sign (Losos et al., 1994). The sphyrnid cephalofoil is formed by latera l expansion of the ro stral, olfactory, and optic regions of the chondrocranium (C ompagno, 1988; Haenni, 2001). The width of the cephalofoil is variable acro ss species, but generally ranges from 18 to 50% of the total length (TL) of the shark (Compagno, 1984). Each species of the eight extant hammerhead sharks has a unique adult head shape (Chapter 1 this dissertation, Figure 2.1) (Gilbert, 1967; Compagno, 1984; 1988; Lim et al., 2010). Sphy rnid sharks are considered to be closely relate d to carcharhinid sharks. Surprisingly, the species with the most expanded cephalofoil ( E. blochii ) represents the most ancestral form and the shark with the least lateral expansion ( S. tiburo ) is the most derived species (Figure 2.1) (Naylor, 1992; Martin, 1993; Martin and Palu mbi, 1993; Lim et al., 2010). Furthermore, new molecular evidence sugge sts that ancestral hammerhead sharks were large bodied and that small body size has evolved at least two times independently (Lim et al., 2010). Because the cephalofoil of sphyrnid sh arks represents such a significant morphological departure from the head mor phology of their sister taxa, the hammerhead sharks (Elasmobranchii, Carcharhiniformes, Sphyrnidae) offer a unique opportunity for studying form and function in an historical context, and addressi ng questions about the evolution of cranial design (Lauder and Liem, 1989; Herrel et al., 2001a; b). The dorsoventrally compressed and laterally expa nded pre-branchial cephalofoil has been the

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80 subject of much speculation but little empirical testing. Reported functions include increased hydrodynamic lift, enhanced binocular vision, greater olfact ory localization and resolution, enhanced electroreception, and pe rhaps a novel mechanism for prey capture (Tester, 1963a; b; Thomson and Simanek, 1977; Compagno, 1984; Johnsen and Teeter, 1985; Strong et al., 1990; Na kaya, 1995; Driver, 1997; Kaji ura, 2001; 2003; Kajiura et al., 2003; 2005; Chapman and Grube r, 2002; McComb et al., 2009). Hammerhead sharks use a number of techniques for capturing prey that do not differ markedly from requiem sharks. The la rger species rely primarily on ram feeding and consume fish (Clarke, 1971; Compa gno, 1984; 1988; Stevens and Lyle, 1989; Wilga and Motta, 2000) while the smaller species us e a combination of ram and suction to consume a wide array of prey species, ranging from crustaceans to fishes (Compagno, 1984; Corts et al., 1996; Wilga and Mo tta, 2000). Some smaller species ( S. media S. tudes and S. tiburo ) include a significant portion of crustaceans in their diet. Two anecdotal studies observed great hammerhead sharks S. mokarran restraining batoid prey with their cephalofoil prior to biting off thei r pectoral fins (Strong et al., 1990; Chapman and Gruber, 2002). Consequently, the biological role of the cephalofoil has also been proposed as a means of prey restrain t in the same manner as juvenile Scyliorhinus canicula use their tail and skin to restrain prey before biting (Southa ll and Sims, 2003). Despite the variation in cephalofoil size and shape, as well as prey types consumed by hammerhead sharks, the functional morphology of the feeding apparatus and prey capture behavior have been described for only one of the eight extant species ( S. tiburo Wilga and Motta, 2000; Mara et al., 2010).

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81 The ability to capture and process food is heavily infl uenced by bite performance in many species. As a result, bite force, a measure of feeding performance, has been extensively studied in verteb rates, including fishes (Wai nwright, 1988; Herrel et al., 2002; Korff and Wainwright, 2004; Grubic h, 2005; Huber et al., 2005; 2009; Kolmann and Huber, 2009; Mara et al., 2010), lizards (Herrel et al., 2001a; Lailvaux and Irschick, 2007), crocodilians (Erickson et al., 2003), birds (van der Meij and Bout, 2000; 2006; Herrel et al., 2005a; b), and ma mmals (Kiltie, 1982; Aguirre et al., 2003; Herrel et al., 2008), and has been linked to the occupati on of novel niches (Hernndez and Motta, 1997; Berumen and Pratchett, 2008) Among the hammerhead sharks, Sphyrna tiburo shows the greatest dietary sp ecialization, having a primarily durophagous diet of portunid crabs in south Florida (Compagno, 1984; Corts et al., 1996; Lessa and Almeida, 1998; Wilga and Motta, 2000; Bethea et al., 2007). Du rophagy in fishes, or the consumption of hard prey, is often associated with hypert rophy of skeletal elements and adductor muscles, larger and more molariform teet h, greater bite force, greater jaw closing mechanical advantage, and a modified biting pattern involving rapid and repeated closure on the prey (Wainwright, 1988; Turingan a nd Wainwright, 1993; Hernndez and Motta, 1997; Clifton and Motta, 1998; Summers, 2000; Huber and Motta, 2004; Summers et al., 2004; Huber et al., 2005). Sphyrna tiburo exhibits few of these functional adaptations for durophagy with the exception of molariform teeth (Wilga and Motta, 2000; Mara et al., 2010). Larger fishes, including sharks, inherently generate larger bite forces because of the larger cross-secti onal areas of their ja w adductor muscles (H uber et al., 2005; 2006; Mara et al., 2010). During the evolution of hamm erhead sharks, with repeated forays into

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82 larger and smaller adult body sizes (Lim et al., 2010), this most likely resulted in differing bite performance. Whether these differe nces translate into differences in feeding niches or differing biologi cal roles of the feeding a pparatus remains unresolved. Given the extreme differences in head size and shape through phylogeny, various constructional constraints are expected wi thin the cephalofoil of hammerhead sharks (Chapter 1; Barel, 1984; Devaere et al ., 2001; Hulsey et al., 2007). Through phylogeny, the internal elements become reorganized to accommodate differences in head shape (Chapter 1). Previous research has demons trated that differences in head shape, particularly dorso-ventral fl attening, can result in constr aints on the position of the feeding apparatus (Devaere et al., 2005). In addition to the probable shifts in feeding performance within the sphyrnid lineage, the question remains whether the sphyrnid feeding bauplan has changed from that of its carcharhinid ancestry as a result of the laterally expanded cephalofoil, or if the feed ing structures have been conserved with morphological changes being confined to the skeletal and sensory structures of the cephalofoil. A study of the feeding morphology and biom echanics of this clade may provide a window into the selective forces and constrai nts that govern cranial design in this unique group of very specialized fishes. Because the cephalofoil of hammerhead sharks represents such a morphological departur e from the head morphology found in other carcharhiniform sharks, it can be used to address the evolution and consequences of changes in head design, and reveal func tional morphological diffe rences among species related to feeding. The goals of this study ar e to: 1) describe and compare the functional morphology and biomechanics of the feeding apparatus of the hammerhead sharks; 2)

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83 investigate if changes to the feeding bauplan exist in sphyrnid shar k or if changes are confined to surrounding structures with cons ervation of the feedi ng apparatus; and 3) investigate the relationshi p between cranial design an d feeding morphology through phylogeny in this clade. MATERIALS AND METHODS Adult individuals of Eusphyra blochii (Cuvier, 1816) (5, 109 – 165.6 cm TL) Sphyrna mokarran (Rppel, 1837) (5, 210 – 399 cm TL), S. zygaena (Linnaeus, 1758) (2, 232 – 293 cm TL), S. lewini (Griffith and Smith, 1834) (5, 246 – 265.5 cm TL), S. tudes (Valenciennes, 1822) (5, 73.5 – 102 cm TL), S. tiburo (Linnaeus, 1758) (5, 85 – 91.5 cm TL), Carcharhinus acronotus (Poey, 1860) (5, 93.5 – 107.5 cm TL), and Rhizoprionodon terraenovae (Richardson, 1836) (5, 85 – 92.6 cm TL) were chosen to represent a continuum of head shape through phylogeny and closely re lated carcharhinid species. Eusphyra blochii were collected in the waters off Darwin, Australia; S. mokarran and S. lewini were collected from various locations along the western and eastern peninsula of S. Florida; S. zygaena were collected from th e eastern coast of S. Florida and the waters off New Zealand; S. tudes was collected off the northeast coast of Trinidad; and S. tiburo C. acronotus and R. terraenovae were collected from the Gulf of Mexico off Sarasota, Florida. Adult specimens were chosen to minimize the effect of ontogeny on head morphology (Haenni, 2001). All animal collection procedures followed the Institutional Animal Care and Use Committee guidelines of Mote Marine Laboratory (08-10-RH1, 07-10-PM 1) and the University of South Florida (T3198, R3205, W3514).

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84 Volumetric Measures The volumetric contributions of the car tilaginous feeding elements (jaws and hyoid) were determined through digitally re constructed computed tomography (CT) as outlined in Chapter 1 (Figure 2.2). Briefly, CT scans were performed on a 64 slice Aquilion Toshiba scanner (Toshiba America Me dical Systems Inc., Tustin, CA, USA) at a 0.5 mm slice interval. Slices were then reconstructed using AMIRA 4.1.2 software (Visage Imaging Inc., San Diego, CA, USA) (Figure 2.2). Feeding Morphology and Bite Force Generation in Sphyrnids The overall organization of the feedi ng system is similar to that of S. tiburo (Wilga and Motta, 2000). The jaw adducting system is composed of four principal muscles the quadratomandibularis dorsal (QMD), quadrat omandibularis ventral (QMV), preorbitalis dorsal (POD), and preorbitalis ventral (POV). The QMD originates on the dorsal surface of the palatoquadrate and travel s posteroventrally to insert on the mid-lateral raphe of the quadratomandibularis complex. The QMV origin ates on the mid-lateral raphe and inserts via a broad fan-like insertion onto the Meckel ’s cartilage. The POD originates on the dorsal surface of the palatoquadr ate just posterior to the orbi tal process and inserts via a tendon onto the mid-lateral raphe. Finally, th e POV originates on the posterior nasal capsule and post-orbital cartilage and travels posterolaterally to merge with the tendon of the POD to insert on the mid-lateral raphe at the corner of the Meck el’s cartilage (Figure 2.3; Wilga and Motta, 2000). For the biomec hanical computations the muscles are considered to insert on the Meckel’s cartilage. Following CT scans, the width of the head, between the distal tips of the cephalofoil, was measured and the skin was removed from both the dorsal and ventral

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85 surfaces of the head ante rior to the first gill slit. The three-dimensional coordinates of the origins and insertions of the muscles i nvolved with jaw adduction, the QMD, QMV, POD, and POV along with the jaw joint and an terior and posterior bite points along the Meckel’s cartilage were obtained using a th ree-dimensional Polhemus Patriot digitizer (Polhemus, Colchester, VT, USA) with the ti p of the rostrum as the center of a threedimensional coordinate system. Each musc le was then unilaterally excised and their mass and volume determined (Figure 2.3) (Wilga and Motta, 2000). Volume was determined by water displacement in a gra duated cylinder and mass on a Brainweigh B 1500 digital scale (Chapter 1). For each musc le the center of mass was determined and the superficial muscle fiber architecture was us ed to estimate the line of action (Huber et al., 2005). The in-lever for each muscle was calculated based on the distance between its insertion on the Meckel’s cartilage and the jaw joint. A resolved in-lever for jaw adduction was then determined from a weight ed average of these individual in-levers based on the proportion of force that each musc le contributed to ove rall force production. Out-lever distances to the ante rior and posterior bite point s were determined from the coordinates of the anterior a nd posterior margins of the f unctional tooth row and the jaw joint. The weighted in-lever was then divi ded by the appropriate out-lever to give the gear ratio for jaw adduction at the anterior (a nterior most tooth) and posterior (posterior most functional tooth) bite points (Huber et al ., 2006; 2008). It is assumed that all skeletal elements act as rigi d beams and mechanical advant age is equivalent to ideal mechanical advantage. The mechanical a dvantage of a jaw adduc ting system indicates the ability of the system to transfer muscle fo rces to prey either rapidly (low mechanical advantage) or forcefully (high mechanical advantage) (Westneat, 2003). Following

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86 excision, each muscle was bisected perpendicu lar to the principal fi ber direction through the center of mass and the cross sectional area was digitized with Sigma Scan Pro 4 (SYSTAT Software Inc., Point Richmond, CA USA) (Huber et al ., 2005). Maximum tetanic tension for each muscle was calculated by multiplying the cross sectional area by the specific tension of elasm obranch white muscle (28.9 N/cm2, Lou et al., 2002). Forces and positions of the origins and insertions were then used to create three-dimensional force vectors for each muscle. Bilateral theoretical maximum bite force at anterior and posterior bite points was th en modeled in 3D with Mathcad 13 (Mathsoft, Inc., Cambridge, MA, USA) by summation of the mo ments generated about the jaw joints by each muscle (Huber et al., 2005). Statistical Analyses All variables were log10 transformed and regressed against TL and studentized residuals input into a princi pal components analysis (PCA ) to investigate the sizeremoved variables resulting in separation among species. Principal components were considered significant if their eigenvalue was greater than 1. In order to determine which variable(s) was the primary determinant of output bite force, two forward stepwise multiple linear regressions were performed with anterior and posterior bite force as dependents. In order to investigate bi te force among sphyrnid and closely related carcharhinid sharks, log10 transformed anterior bite for ce values were regressed against log10 shark TL to remove the effect of size. Average residual data for each species was then qualitatively compared. To account for the phylogenetic non-inde pendence of the data, independent contrasts for all log10 transformed variables were ge nerated using the most recent

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87 sphyrnid phylogeny which includes branch leng ths (Lim et al., 2010; Martin, 1993) using Mesquite 2.72 (Maddison and Maddison, 2009). Feeding morphology data collected here were combined with volume data collected previously (Chapter 1) in the phylogenetic analysis. Because this phyloge ny includes only a single outgroup, C. acronotus was retained as the outgroup species for phylogene tic analyses. In order to account for the large size range of the species studied here, the contrast value for each of the variables was then regressed, through the origin, against the contrast of TL. The studentized residuals were then analyzed with a Pearson co rrelation analysis, th rough the origin. Correlation analyses reveal the relationship between pairs of va riables. Finally, Mesquite was used to perform ancestral state characte r reconstructions to i nvestigate how feeding variables change through evol utionary history, as describe d in Chapter 1. Regressions and the PCA analysis were performed in SYSTAT v11 (SYSTAT Software Inc., Chicago, IL, USA) and the correlation an alysis was performed in SPSS v18 (SPSS, Chicago, IL, USA). RESULTS Feeding Morphology and Biomechanics Principal components analysis revealed that species separate based on a combination of mass and force of the jaw cl osing musculature and bite force. Two significant principal components (eigenvalue > 1) were retain ed for further analysis. Together these two principal components e xplained 78.9% of the va riation in feeding morphology within hammerhead sharks. Prin cipal component 1 explained 49.7% of the variation and represents increasi ng values of anterior and post erior bite force, along with

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88 QMV and QMD mass and force. Principa l component 2 explained 27.2% of the variation, and represen ts increasing values of POV a nd POD mass and force (Figure 2.4). Carcharhinid outgroups ( C. acronotus and R. terraenovae ) along with S. mokarran had among the largest size-removed bite forces or largest muscle masses and forces. Whereas E. blochii S. lewini and S. tiburo displayed among the lowest size-removed bite forces, muscle masses, and muscle forces. Similarly, S. tudes and S. tiburo displayed relatively large values for POV and POD mass and fo rce (Figure 2.4). Principal components analysis indicated that all va riables contributed significantly to separation among species, and as a result, all variables were retained for further analyses. The raw data indicate that the masses and volumes of the feeding muscles and cartilages varied among species (Table 2.1, 2.2, Figure 2.5). The Meckel’s cartilage was consistently larger in volume than the pa latoquadrate in all species (Table 2.2). Consequently, the muscles that rest upon each cartilage follow ed similar trends with the QMV having a greater mass than the QMD (Table 2.1). Both anterior (18.2 – 642.22 N) and posterior (71.08 – 1839.43 N) absolute bite force spanned a full order of magnitude (Table 2.1). Within sphyrnid sharks mechanical advantage ranged from 0.12 – 0.26 at the anterior bite point and from 0.76 – 1.01 at th e posterior bite point. Out-groups showed similar but slightly higher anterior and posterior mechanical advantage (0.3 – 0.33 and 1.18 respectively). Sphyrna zygaena had the smallest (0.12) anterior mechanical advantage while E. blochii and S. mokarran had the largest (0.26) i ndicating a more force efficient jaw in E. blochii and S. mokarran Posterior mechanical advantage was smallest in S. lewini (0.88) and largest in S. zygaena (1.01) (Table 2.1).

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89 Multiple linear regression of size-removed da ta indicated that the best predictor of output anterior bite force for sphyrnid a nd outgroup carcharhinid sharks was the force produced by the POV (p = 0.029). For posterior bite force the best predictors include POV force (p < 0.001), POD force (p = 0.001), a nd posterior mechanical advantage (p < 0.001). Furthermore, the QMV consistently produced the greatest proportion of overall muscle force in all species (Table 2.3). Although size-removed analyses of bite force data provide little information without phylogeny being taken into account, it is sometimes instructive to qualitatively compare size-removed bite force among species, in this case within sphyrnid sharks. The regression of log anterior bite force vs. log10 shark TL indicates that species cluster relatively close together (Log ABF = 2.144(Log TL) – 2.705, Figure 2.6). However, species form clear groups both above and belo w the regression line (Figure 2.6) with the range of residual bite force falling both a bove and below predictions (Table 2.4). Eusphyra blochii S. zygaena and S. tiburo all have anterior bite force values that fall below predicted values with average residu als of -0.77, -1.26, and -1 .22 respectively. Furthermore, the range of residual values for E. blochii S. zygaena and S. tiburo indicates that anterior bite force for all individuals sampled for these species fell well below predicted (negative residual ranges) (Table 2.4). When sphyrnid sharks are compared to carcharhinid sharks, both carcharhinid sharks, C. acronotus and R. terraenovae have higher than predicted bite for ces with average residuals of 1.18 and 0.66 respectively. Sphyrna mokarran is the only hammerhead to have consistently higher than predicted bite forces with an averag e residual bite force of 0.87 (Figure 2.6, Table 2.4).

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90 Changes among Feeding and Sensory Structures Pearson correlation analyses of the feeding morphology, bite force, and volume of the internal components of the cephalofoil indicate that much of the cephalofoil is morphologically conserved with few correlatio ns found between elements. The feeding variables showed both positive and negative correlations. Positive correlations were particularly apparent in the volume of the f eeding apparatus and muscles. Furthermore, as the palatoquadrate increased in volume the Meckel’s car tilage also increased in volume. The volume of the hyomandibula a nd ceratohyal also displayed this same relationship with palatoquadrate and M eckel’s cartilage volume (Table 2.5). Similar to the internal volumes, both positive and negative correlations were concentrated in the masses of the principa l jaw closing muscles (QMV, QMD, POV, and POD) with fewer correlations relating to th e jaw and jaw suspension cartilages (Table 2.5). However, as the number of variables being analyzed increases, the chance of spurious correlations increases (Aldrich, 1995) Consequently, correlations such as that of the eye and ceratohyal size are most lik ely meaningless. Correlations will only be addressed if the elements are adjacent or ne arby structures as per the definition of constraints utilized in Chapter 1. A numb er of both positive and negative correlations were found among volume and feeding morphol ogy variables. Positive correlations included anterior mechanical advantage being positively corr elated with POV, palatoquadrate, Meckel’s cartilage, and hyomandibula volumes, indicating more force efficient bites are correlated with increa sing volumes of the POV, palatoquadrate, Meckel’s cartilage, and hyomandibula. Po sterior mechanical advantage was also positively correlated with posterior bite for ce. The remaining positive correlations are

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91 confined to the feeding muscles (masses and fo rces). Anterior bite force was positively correlated with POD mass and force and POV force. The four principal jaw closing muscles also display various positive correlations among each other. The QMV mass is positively correlated with the masses of the QMD and POV, and the force produced by the QMD. The mass of the QMD showed the same pattern as QMV with positive correlations associated with QMV and POV mass and QMD force. The masses of the POV and POD are positively correlated with POV force with POV mass also being correlated with QMD and POD force. Fi nally, POV and POD force are positively correlated with each other (Tab le 2.5). These correlations i ndicate that as anterior bite force increases the mass and force of the POD and the force of the POV also increase, but not the masses of the QMD and QMV. In terestingly, a positive correlation was also found between nasal capsule volume and the mass of the QMV and QMD indicating that as nasal capsule volume increased the mass of the QMV and QMD also increased. Similarly, a positive correlation between nasal capsule volume and volume of the QMD was also detected (Table. 2.5). While many variables were positively correlated, there were negative correlations among variables too. Posterior bite force wa s negatively correlated with the volumes of the POV, POD, palatoquadrate, Meckel’s ca rtilage, and hyomandibula. These negative correlations indicate, somewhat paradoxically, that as poster ior bite force increases the volume of the POV, POD, palatoquadrate, Meckel’s cartilage, and hyomandibula decrease. Similarly, the volume of the ba sihyal was negatively correlated with the masses of the QMV, QMD and POD along with the force of the QMD. Both the chondrocranium and total volume had the same pattern of negative co rrelations as the

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92 basihyal indicating that as jaw adductor muscle masses get larger the basihyal, chondrocranium, and total volume decrease in size. Lastly, the posterior mechanical advantage was negatively correlated with the force of the POD indicating that as posterior mechanical advantage increased the force produced by the POD decreased (Table 2.5). Ancestral State Reconstructions The primary ancestral node of interest is the split between the extreme lateral expansion seen in Eusphyra (up to 50% of TL) and the relatively moderate expansion seen in Sphyrna (less than ~27% of TL) (Node 3 Fi gure 2.1). This node represents the most common ancestor to Eusphyra and Sphyrna This ancestor is intermediate in both TL and lateral expansion (~179.08 cm and 46.64 cm or ~26% of TL respectively) (Figure 2.1, Table 2.1 and 2.6) and is characterized by in termediate anterior and posterior bite force (Table 2.1 and 2.6). Through evolutionary history of the sphyrni ds, the general trend is for the mass of the POV to be greater than that of the re maining feeding muscles. However, the QMV consistently produces the most force despit e not being a significant predictor of output bite force in extant taxa. Both anterior a nd posterior mechanical advantages were similar through evolutionary history and not different than exta nt taxa (Table 2.1 and 2.6). DISCUSSION Feeding Morphology and Biomechanics When compared to closely related carcha rhinid sharks, the feeding morphology of sphyrnid sharks is not markedly different. Furthermore, cep halofoil width did not have a

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93 significant effect on feeding morphology and bite force. Sphyrnid and carcharhinid sharks, both carcharhiniform sharks, have similar anatomical arrangements of the quadratomandibularis and preorbitalis muscles, have similar jaw protrusion mechanisms, and even share similar jaw motor patte rns (Moss, 1977b; Compagno, 1988; Wilga and Motta, 2000; Motta et al., 1997; Huber et al., 2006). Despite changes to the chondrocranium and sensory structures as a result of evolution of the cephalofoil, the feeding bauplan remains unchanged in sphyrnid sharks compared to carcharhinid species (Table 2.1, Figure 2.5). The mechanical advantage of the jaw clos ing system provides an estimation of the ability of the feeding system to transmit muscle forces to either speed efficient (mechanical advantages closer to 0) or for ce efficient (mechanical advantages close to and greater than 1.0) jaw closure (Westneat, 1994; 2003; Cutwa and Turingan, 2000; Wainwright and Shaw, 1999; Wainwright an d Richard, 1995; Wainwright, 1999). In particular, if the mechanical advantage is greater than 1.0, the system switches from a class three to a class two lever system. Cla ss three lever systems include those where the in-lever is less than or equal to the out-lever resulting in output forces less than or equal to the input muscle forces. However, second class lever systems are force amplifying and have an in-lever that is greater than the out-l ever. In second class lever systems, the input muscle force is amplified resulting in larger output forces and a force efficient jaw closing system. This may be possible for posterior teeth where the adductor muscle inserts anterior to these t eeth (Durie and Turingan, 2001; Wa inwright and Richard, 1995; Turingan et al., 1995; Hernndez and Motta 1997; Huber, 2006; Huber et al., 2005; 2008; Mara et al., 2010).

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94 Mechanical analysis of the feeding morphology indicates that sphyrnid and closely related carcharhinid sharks posses bot h class two and class three lever systems with most sphyrnid sharks having posterior mechanical advantages less than 1.0, and closely related carcharhinid sharks having poste rior mechanical advantages greater than 1.0 (Table 2.1). Force amplifying systems with mechanical advantages greater than 1.0 have been previously found in both chondricht hyan oral and teleost oral and pharyngeal jaws (horn shark Heterodontus francisci spotted ratfish Hydrolagus colliei, black drum, Pogonia cromis and striped burrfish, Chilomycterus schoepfi ) (Korff and Wainwright, 2004; Huber et al., 2005; Grubi ch, 2005; Huber et al ., 2008). All of these fishes are durophagous; however, posterior m echanical advantages greater than one have also been found in piscivorous species su ch as the black tip shark, Carcharhinus limbatus (Huber et al., 2006). The implications of changes in m echanical advantage to jaw suspension have been described in detail (Hube r, 2006). With increasing valu es of posterior mechanical advantage, the forces acting on the jaw join t switch from compression, which pushes the upper and lower jaws together, to tension, which attempts to pull them apart. This switch to a jaw joint in tension results in greater chance for dislocation which is resisted by robust ligamentous connections (Motta and W ilga, 1995; Huber, 2006; Huber et al., 2008). Compared to outgroup carcharhinid sharks (anterior and posterior mechanical advantages of 0.3 – 0.33 and 1.18 respectively) sphyrnid sharks had lower values for both anterior and posterior mechanical advantag e. The anterior mechanical advantage for sphyrnid sharks ranged from 0.12 in S. zygaena to 0.26 in E. blochii and S. mokarran Posterior mechanical advantage also va ried among sphyrnid sharks from 0.76 in S. lewini

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95 to 1.01 in S. zygaena (Table 2.1). Furthermore, the an terior mechanical advantage of sphyrnid sharks places them with numerous te leost fishes with low to intermediate jaw leverages, including wrasses ( 0.13 – 0.41) and gray triggerf ish (0.25 – 0.27) (Durie and Turingan, 2001; Wainwright et al., 2004; Westneat, 2004). Sphyrnid shark anterior mechanical advantage is considerably smalle r than that found in durophagous fish such as the horn shark (0.51), chimaera (0.68), and pa rrotfish (0.45 – 1.04) (Wainwright et al., 2004; Huber et al., 2005; 2008). Speed efficien t jaws are often found in organisms that consume elusive prey, such as fish (Westn eat, 2004). The speed e fficient jaw closing system found in sphyrnid sharks is not that surprising when th e diet of sphyrnid sharks is taken into account. Most hammerhead sharks consume primarily fish and squid (up to 82.9% and 68.9% of diet, respectively). Sphyr nid sharks will also include hard prey (decapod crustaceans) in their diet with some species, such as S. tiburo consuming almost exclusively hard prey (Corts, 1999; Corts et al., 1996; Bethea et al., 2007). Sphyrna tiburo capitalizes on their hard portunid prey by mostly limiting their diet to crabs that they are capable of crushing with their posterior molariform teeth (Mara et al., 2010; Chapter 3) and by utilizing speciali zed motor patterns (Wilga and Motta, 2000). Despite these apparent modifications for durophagy, this species does not display many of the characteristics of other durophagous chondrichthyans, such as robust reinforced jaws, hypertrophied feeding muscles, and fu sed jaw symphyses (Mara et al., 2010; Wilga and Motta, 2000). In order to gain a more complete understanding of the feeding morphology of a species, mechanical advantag e should not be considered alone, but as part of a larger system including muscle a ngles and force production in addition to lever arms (De Schepper et al., 2008).

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96 The best predictor of output anterior bite force was the force produced by the POV. Similarly, posterior b ite force was best predicted by the force produced by both the POV and the POD along with posterior mechani cal advantage (Table 2.3). These results contradict previous studies that found the quadratomandibul aris complex of muscles is the best predictor of output force in both Heterodontus francisci and S. tiburo (Huber et al., 2005; Mara et al., 2010). While the reason for this discrepancy remains unclear, it is possible that the lateral expansi on of the nasal capsule plays a ro le in this difference. As the nasal capsule expands laterally, the origin of the POV on the posterior nasal capsule (Wilga and Motta, 2000) is nece ssarily modified and expande d resulting in a greater cross-sectional area, leading to the trend of greater force pr oduction in sphyrnid sharks as compared to outgroup carcharhinids (Figure 2.5; Table 2.1). However, confounding these results is the fact that the POV has b een shown to be active during jaw protrusion with activity ceasing at full jaw closure (Wilga and Motta, 2000). That the POD significantly predicts posterio r bite force is surprising given the morphology of this muscle. The POD has a much broader origin on the upper jaw compar ed to carcharhinid species (note: during jaw protrusion this switches to the insertion for the POD) and inserts onto the mid-lateral raphe of the quadratomandibularis muscle complex at a similar shallow angle to the POV (Wilga and Motta, 2000). Static equilibrium models predict that when muscles insert at a more or thogonal angle to the lo wer jaw, more of the force produced by that muscle wi ll be transmitted in the dors o-ventral plane, resulting in increased contribution to output bite force. Consequently, the quadratomandibularis complex better predicts posterior bite force in other carcharhiniform sharks (Huber et al., 2005; Mara et al., 2010).

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97 While absolute bite force values allow for comparisons among species, size often confounds this type of analysis. Size-re moved analyses allow for intraspecific comparisons of disparate taxa of varying size ranges (Herrel et al., 2004; 2007; Huber et al., 2005; Mara et al., 2010). However, size or mass specific comparisons of bite force should be interpreted cautiously. The reason fo r this is the method of size removal. In order to perform size-removed comparisons, bite force is linearly regressed against either length or mass of the individuals. In this type of analysis, if one or more individuals have exceptionally high or exceptionally low bite fo rce for their length or mass, the regression line and consequently the residu al data will be heavily infl uenced by these outliers. Furthermore, exceptionally elongated taxa (e .g. elongated caudal fin of orectolobiform or alopiid sharks) may bias the in terpretation. To avoid this prob lem, this study investigated size-removed data from only within sphyrnid and closely related ca rcharhinid species (Figure 2.6, Table 2.4). Tota l length removed residual bite force reveals that among sphyrnid and closely related carcharhinid species, E. blochii S. zygaena and S. tiburo all have an average residual anterior bite force that is less than predicted (-0.77, -1.26, and 1.22 respectively) (Table 2.4). While the nega tive average residual values are not that surprising for the piscivorous E. blochii and S. zygaena (Compagno, 1984), the negative residuals of S. tiburo are surprising given the proportion of hard prey incl uded in its diet (up to 85% IRI) (Corts et al., 1996). Dietary and bite perfor mance data indicate that, at least in South Florida, S. tiburo primarily consumes Callinectes sapidus it is capable of crushing. Crabs falling outside th e maximum crushing abilities of S. tiburo are found in the stomachs indicating that some method of prey processing other than crushing is employed to consume crabs of this size (Mar a et al., 2010; Chapter 3). Sphyrnid sharks

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98 generally had smaller average residual bite force than outgroup ca rcharhinid species (Table. 2.4), and both C. acronotus and R. terraenovae had higher than predicted residual anterior bite force values (1.18 and 0.66 respectively). The lone sphyrnid with comparable average residual bite force to outgroup carcharhinids was S. mokarran with an average of 0.87 (Figure 2.6, Table 2.4). An integral part of the feeding system that is often overlooked is the morphology and biomechanics of the teeth. Biom echanical analyses reveal that S. mokarran teeth perform poorly at puncturing soft prey, but are able to be un ilaterally draw n through prey with little force once puncture has occu rred (Whitenack, 2008; Whitenack and Motta, 2010). The teeth of S. mokarran are typical for carcharhinifom species, with moderately long central cusps that are strongly serra ted anteriorly and cu spidate posteriorly (Compagno, 1984). The teeth of S. mokarran have cusps that are slightly inclined toward the back of the jaws resulting in poor perf ormance during puncture testing (Whitenack, 2008). Sphyrna zygaena S. lewini S. tudes have teeth similar to S. mokarran in appearance, however, their anterior teeth are only weakly serrated. Sphyrna tiburo has anterior teeth that lack serrations and posteri or teeth that are molariform allowing for the consumption of hard prey (Compagno, 1984; Corts et al., 1996; Wilga and Motta, 2000; Mara et al., 2010). Given the shape and performance of sphyrnid teeth (Whitenack, 2008), it is expected that la rge bodied sphyrnids with strongly serra ted and posteriorly inclined teeth similar to S. mokarran would employ lateral head shaking to process their prey and would display relatively larger bite forces to counteract the inertia of the prey during lateral shaking. Sphyrna mokarran has been observed usin g lateral head shaking

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99 to remove pieces of prey (K.R. Mara persona l observation; Strong et al., 1990; Chapman and Gruber, 2002). The evolution of jaw suspension in chondrichthyes has been thoroughly investigated (e.g. Wilga, 2002; 2005; 2010; Wilga et al., 20 07; Huber, 2006). Sphyrnid and other carcharhiniform species have a hyostylic jaw suspension, which allows for extensive palatoquadrate protrusion (Wilg a and Motta, 2000; Wilga, 2002; 2010). The degree of jaw protrusion is primarily dete rmined by the length or absence of the ethmopalatine ligament; as well as the le ngth and orientation of the cartilaginous elements of the suspensory apparatus (W ilga, 2005; 2010; Wilg a et al., 2007). Furthermore, the orientation of the hyoma ndibula differs among elasmobranchs and can be linked to feeding style (Moss, 1977a; b), with posteriorve ntrally directed hyomandibulae being related to bite feeders such as carcharhiniform and lamniform sharks (Wilga, 2008; 2010). Within Sphyrnidae, the hyomandibulae are posteriorventrally directed (see Chapter 1 Figure 1.12, Figure 2.5), facilitating a biting method of prey capture (Wilga and Motta, 2000). Furthermore, in S. tiburo there is minimal protrusion due to a relatively shor t ethmopalatine ligament (Wilga and Motta, 2000; Motta and Wilga, 2001). While minimal jaw protrusion may be advantageous for the durophagous S. tiburo the remaining piscivorous species would be expected to have larger jaw protrusion distances. However, this remains to be tested in other sphyrnid species (Wilga and Motta, 2000 ; Motta, 2004). A study qua ntifying the protrusion distance and kinematics of sphyrnid shar ks would help elucidate the potential consequences of lateral head expansion on feeding kinematics and jaw protrusion in sphyrnid species.

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100 Changes among Feeding and Sensory Structures Previous research has indicated that the position and shape of the mouth is constrained within sphyrnid sharks. The jaw cartilages and the muscles that rest upon them change in concert with each other through phylogeny (Cha pter 1). The morphology of the feeding apparatus has been described for S. tiburo (Wilga and Motta, 2000; Mara et al., 2010) and is consistent within the rest of the family. Differences in tooth morphology do exist among hammerhead sharks and are apparently related to biomechanical performance and differences in diet (Compagno, 1984; 1988; Whitenack and Motta, 2010). The volumes of the sensory, neural, and supportive structures within the cephalofoil showed both positive and negati ve correlations. The volumes of the palatoquadrate and Meckel’s cartilages were po sitively correlated with the volumes of the jaw closing musculature. Negative correlations within the cephalofoil were found between nasal capsule and brai ncase, chondrocranium, and to tal volume. Similarly, eye volume displayed a negative correlation to he ad width, indicating th at as head width increases, eye volume decreases (Chapter 1). Within sphyrnid and closely related carch arhinid species, changes in feeding morphology are independent of changes in he ad width. Changes in the volume of the feeding muscles are positively correlated with changes in the cartilaginous feeding elements (Table 2.5). Similarly, the masses and forces produced by the various feeding muscles also displayed positive correlations among each other. Positive correlations were detected between anteri or mechanical advantage an d the volumes of the POV, palatoquadrate, Meckel’s car tilage and hyomandibula (Table 2.5). This indicates that

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101 more force efficient anterior bites are associ ated with increases in the volume of these correlated elements. Anterior bite force was also positively correlated with the mass of the POD and the force of the POD and POV. That anterior bite force is positively correlated with the force produced by the POV is not surprising given that this variable is the primary predictor of anterior bite force (Table 2.3). More force efficient posterior biting is correlated with incr easing posterior bite force valu es, which is consistent with predictions of increasing mechanical adva ntage being related to increased force production (Durie and Turingan, 2001; Wain wright et al., 2004; Westneat, 2004). Pearson correlation analysis revealed th at there are negative correlations among feeding morphology variables thro ugh evolutionary history (T able 2.5). Particularly striking, is the negative correlation between posterior bite force and the volume of the POV, POD, palatoquadrate, Meckel’s cartilage, and hyom andibula. These negative correlations contradict predicti ons for the structural conseque nces of increasing posterior bite force (Summers, 2000; Summers et al., 200 4; Huber et al., 2005), and may be related to the orientation of the muscles and thei r primary role in jaw protrusion (Wilga and Motta, 2000). Specifically, the POV and P OD may insert at a more acute angle to facilitate palatoquadrate protrusion, conseque ntly reducing their orthogonal component of force that contributes to jaw a dductive bite force. It should also be noted that the volume of a muscle does not necessarily reflect its cr oss sectional area. While the volume of the muscle may decrease, muscle width may incr ease resulting in increased cross sectional area and consequently increased force. S upporting this, in sphyrni d and closely related carcharhinid sharks the force produced by th e POV and the POD, not the volumes, are the best predictors of posterior bite force.

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102 Sphyrnid sharks also displayed negative correlations between the volume of the basihyal and the masses of the QMV, QMD, and POD along with the force produced by the QMD (Table, 2.5). Unlike the jaw closing musculature, the primary role of the basihyal is to transmit jaw abductive muscle fo rce to the Meckel’s cartilage, such as occurs during jaw opening. Furthermore, hypertrophy of the jaw abducting musculature in specialized suction feeders (Ramsay a nd Wilga, 2006) could result in increased volume of the basihyal. Convers ely, in biting-speci alized species wher e the generation of suction pressure is not as important, the sele ctive pressure for a larger basihyal could be reduced. Another negative corr elation is that of the poste rior mechanical advantage which is negatively correlated with the forc e produced by the POD. Again, this negative correlation is somewhat surprising given the POD’s function in jaw closure. Multiple linear regression indicated that the force generated by the POD was one of the best predictors of posterior bite force (Table 2.3) This negative correlation may be the result of changes to the mechanical advantage or mu scle architecture among species. Either the out-lever becomes shorter or the weighted in-lever becomes longer resulting in an increase in mechanical advantage. The relationship between posterior mechanical advantage and the force produced by the P OD could also be heavily influenced by S. mokarran which possesses a relatively large P OD muscle force and among the lowest posterior mechanical advantages. Sphyrna mokarran may have a relatively shorter outlever as a result of a relatively shorter palatoqua drate or a relatively longer in-lever as a result of changes in the insertion points of the adductive musculature for this species. This negative correlation could also be the result of changes to the insertion point or angle for the POV. If the POV is modified to insert at a more ort hogonal angle, more of

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103 the force it produces would be ut ilized for bite force. Chan ging the insertion angle would necessitate a change in insert ion point thereby modifying the lever mechanics. Raw data point to an inverse trend between mechanical advantage and POV and POD cross sectional area (force) (Table 2.1) In sphyrnid sharks, this ma y be due, in part, to the increased lateral cephalofoil expansion resultin g in a larger origin and consequently a larger cross sectional area for the POV (Table 2.1). This correlation analysis i ndicates that as th e head of sphyrnid sharks expands and contracts laterally through phylogeny, there ar e few constraints on the feeding apparatus imposed by the adjacent non-feed ing structures. What cons traints exist are among the various feeding structures. This is expected because of their comm on biological role in feeding and prey capture. The closest co mmon ancestor to all sphyrnid sharks was intermediate in lateral cepha lofoil expansion (~26% of TL) and relatively large bodied (~179.08 cm TL) (Figure 2.1, Table 2.6 Node 3). Recent phylogenetic analyses indicate that modern sphyrnid sharks are the result of divergent evolutionary process resulting in a lineage of sphyrnids displaying cephalofoil expansion ( Eusphyra lineage with cephalofoil expansion up to 50% of TL) and a second displaying cephalofoil contraction ( Sphyrna lineage with cephalofoil expans ion up to 27% of TL) (Figur e 2.1, Table 2.6 Node 3) (Lim et al., 2010). The predictions of a large bodi ed ancestral sphyrnid presented here match those of Lim et al. (2010). This study found that the contribution of the QMV to overall force production was similar through evolutionary history matc hing results from previous studies showing that this muscle consistently produces the greatest proportion of overall force (Mara et al., 2010). Finally, the reconstr ucted anterior and posterior mechanical advantages match

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104 those of the extant taxa. Th is indicates that through much of their evolutionary history sphyrnid sharks had speed efficient jaw clos ing systems and their diet likely consisted largely of elusive prey. CONCLUSIONS Within sphyrnid sharks the feeding baupl an is conserved with few changes to feeding structures or feeding biomechanics. Furthermore, changes to the cephalofoil are mainly confined to the sensory structures. The mechanical advantage of the jaw closing system within sphyrnids is similar to the sp eed efficient jaw closi ng systems of fishes with low to intermediate jaw leverages. That a speed efficient jaw closing system was found among sphyrnid sharks is not surprising given the primarily elusive diet of these species. Multiple linear regression indicated that the best predictor of anterior bite force was the force produced by the POV, while posterior bite force is best predicted by the force of both the POV and POD along with the posterior mechanical advantage. Surprisingly, the lone durophagous me mber of the family Sphyrnidae, S. tiburo had among the lowest length sp ecific bite forces. This analysis also revealed that cha nges in cephalofoil width had no effect on feeding morphology. Within sphyrnid and closel y related carcharhinid sharks increasing anterior mechanical advantage is associ ated with increased volume of the POV, palatoquadrate, Meckel’s cartilage and hyoma ndibula. Similarly, increasing posterior mechanical advantage was positively correlated with increasing posterior bite force. These positive correlations are most likely re lated to structural modifications to the feeding structures rela ted to increased bite force produc tion and transmission. Posterior

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105 bite force was negatively correlated with th e volume of the POV, POD, palatoquadrate, Meckel’s cartilage, and hyoma ndibula, despite these struct ures’ role in feeding. However, posterior bite force is best pr edicted by the force produced by the POV and POD not the volume occupied by these muscles. Raw data also show an inverse trend between posterior mechanical advantage and the force produced by the POV and the POD, indicating that the increased expansion of the nasal capsule found in sphyrnid sharks may result in an increased cross sectional area and increased force in the POV. Ancestral state reconstructions were found to match those predicted by other studies regarding ancestral sphyrnid size and head width, indicating that the ancestral sphyrnid shark was relatively large bodi ed with a moderately expande d cephalofoil. These data indicate that much of the sphyrnid head is conserved through phylogeny. LITERATURE CITED Adriaens, D. and Herrel, A. (2009). Functional consequences of ex treme morphologies in the craniate trophic system. Physiological and Biochemical Zoology 82 1-6. Aguirre, L. F., Herrel, A., Va n Damme, R., and Matthysen, E. (2003). The implications of food hardness for diet in bats. Functional Ecology 17 201-212. Aldrich, J. (1995). Correlations genuine and spurious in Pearson and Yule. Statistical Science 10 364-376. Barel, C. D. N. (1984). Form-relations in the contex t of constructional morphology: the eye and suspensorium of lacustrine Ci chlidae (Pisces, Teleostei): with a discussion on the implications for phyloge netic and allometric form-interactions. Netherlands Journal of Zoology 34 439-502. Berumen, M. L. and Pratchett, M. S. (2008). Trade-offs associated with dietary specialization in corallivorous butterflyfishes (Chaetodontidae: Chaetodon ). Behavioral Ecology and Sociobiology 62 989-994. Bethea, D. M., Hale, L., Carlson, J. K., Co rts, E., Manire, C. A., and Gelsleichter, J. (2007). Geographic and ontogenetic variatio n in the diet and daily ration of the

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111 Motta, P. J. (2004). Prey capture behavior and feed ing mechanics of elasmobranchs. In Biology of Sharks and Their Relatives Eds. J. Carrier J. Musick and M. Heithaus, pp. 165-202. Boca Raton: CRC Press LLC. Motta, P. J. and Wilga, C. A. D. (1995). Anatomy of the feed ing apparatus of the lemon shark, Negaprion brevirostris Journal of Morphology 226 309-329. Motta, P. J. and Wilga, C. D. (2001). Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environmental Biology of Fishes 60 131156. Motta, P. J., Tricas, T. C., Hueter, R. E., and Summers, A. P. (1997). Feeding mechanism and functional morphology of the jaws of the lemon shark Negaprion brevirostris (Chondrichthyes, Carcharhinidae). Journal of Experimental Biology 200 2765-2780. Nakaya, K. (1995). Hydrodynamic function of the head in the hammerhead sharks (Elasmobranchii: Sphyrnidae). Copeia 1995 330-336. Naylor, G. J. P. (1992). The phylogenetic relationshi ps among requiem and hammerhead sharks: inferring phylogeny when thousands of equally most parsimonious trees result. Cladistics 8 295-318. Ramsay, J. B. and Wilga, C. D. (2006). Hyoid mechanics and muscle function during feeding in white-spotted bamboo sharks. Society of Integrative and Comparative Biology 46 e114. Shirai, S. and Nakaya, K. (1992). Functional morphology of feeding apparatus of the cookie-cutter sharks, Isistius brasiliensis (Elasmobranchii, Dalatiinae). Zoological Science 9 811-821. Southall, E. J. and Sims, D. W. (2003). Shark skin: a function in feeding. Proceedings of the Royal Society of London B 270 S47-S49. Stevens, J. D. and Lyle, J. M. (1989). Biology of three hammerhead sharks ( Eusphyra blochii, Sphyrna mokarran, and S. lewini ) from northern Australia. Australian Journal of Marine and Freshwater Research 40 129-146. Strong Jr., W. R., Snelson, F. F., and Gruber, S. H. (1990). Hammerhead shark predation on stingrays: an obs ervation of prey handling by Sphyrna mokarran Copeia 1990 836-840. Summers, A. P. (2000). Stiffening the stingray skel eton an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). Journal of Morphology 243 113-126.

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112 Summers, A. P., Ketcham, R. A., and Rowe, T. (2004). Structure and function of the horn shark ( Heterodontus francisci ) cranium through ontogeny: development of a hard prey specialist. Journal of Morphology 260 1-12. Tester, A. L. (1963a). The role of olf action in shark predation. Pacific Science 17 145170. Tester, A. L. (1963b). Olfaction, gestation and the co mmon chemical sense in sharks. In Sharks and Survival Ed. P. W. Gilbert, pp. 255-285. Boston: C.C. Heath and Company. Thomson, K. S. and Simanek, D. E. (1977). Body form and locomotion in sharks. American Zoologist 17 343-354. Turingan, R. G. and Wainwright, P. C. (1993). Morphological and functional bases of durophagy in the queen triggerfish, Balistes vetula (Pisces, Tetraodontiformes). Journal of Morphology 215 101-118. Turingan, R. G., Wainwright, P. C., and Hensley, D. A. (1995). Interpopulation variation in prey use a nd feeding biomechanics in Caribbean triggerfishes. Oecologia 102 296-304. van der Meij, M. A. A. and Bout, R. G. (2000). Seed selecti on in the Java sparrow ( Padda oryzivora ): preference and mechanical constraint. Canadian Journal of Zoology 78 1668-1673. van der Meij, M. A. A. and Bout, R. G. (2006). Seed husking time and maximal bite force in finches. Journal of Experimental Biology 209 3329-3335. Wainwright, P. C. (1988). Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69 365-645. Wainwright, P. C. (1999). Ecomorphology of prey capture in fishes. In Ichthyology Recent Research Advances Ed. D. N. Sakesena, pp. 403-415. New Delhi: Oxford & IBH Publishing Co. Wainwright, P. C. and Richard, B. A. (1995). Predicting patte rns of prey use from morphology of fishes. Environmental Biology of Fishes 44 97-113. Wainwright, P. C. and Shaw, S. S. (1999). Morphological basis of kinematic diversity in feeding sunfishes. Journal of Experimental Biology 202 3101-3110. Wainwright, P. C., Bellwood, D. R., West neat, M. W., Grubich, J. R., and Hoey, A. S. (2004). A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biological Journal of the Linnean Society 82 1-25.

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113 Westneat, M. W. (1994). Transmission of force and ve locity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes). Zoomorphology 114 103-118. Westneat, M. W. (2003). A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223 269281. Westneat, M. W. (2004). Evolution of levers and linkages in the feeding mechanisms of fishes. Integrative and Comparative Biology 44 378-389. Whitenack, L. B. (2008). The biomechanics and evolution of shark teeth. pp. 354. Dissertation. University of South Florida, Tampa, FL. Whitenack, L. B. and Motta, P. J. (2010). Performance of shark teeth during puncture and draw: implications fo r the mechanics of cutting. Biological Journal of the Linnean Society 100 271-286. Wilga, C. D. (2002). A functional analysis of jaw suspension in elasmobranchs. Biological Journal of the Linnean Society 75 483-502. Wilga, C. D. (2005). Morphology and evolution of the jaw suspension in lamniform sharks. Journal of Morphology 265 102-119. Wilga, C. A. D. (2008). Evolutionary divergence in the feeding mechanism of fishes. Acta Geologica Polonica 58 113-120. Wilga, C. D. (2010). Hyoid and pharyngeal arch f unction during ventilation and feeding in elasmobranchs: conservation and modification in function. Journal of applied Ichthyology 26 162-166. Wilga, C. D. and Motta, P. J. (1998a). Conservation and variation in the feeding mechanism of the spiny dogfish Squalus acanthias Journal of Experimental Biology 201 1345-1358. Wilga, C. D. and Motta, P. J. (1998b). Feeding mechanism of the Atlantic guitarfish Rhinobatos lentiginosus : modulation of kinematic and motor activity. Journal of Experimental Biology 201 3167-3184. Wilga, C. D. and Motta, P. J. (2000). Durophagy in sharks : feeding mechanics of the hammerhead Sphyrna tiburo Journal of Experimental Biology 203 2781-2796. Wilga, C. D., Motta, P. J., and Sanford, C. P. (2007). Evolution and ecology of feeding in elasmobranchs. Integrative and Comparative Biology 47 55-69.

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114 Wu, E. H. (1994). Kinematic analysis of jaw prot rusion in Orectolobiform sharks: a new mechanism for jaw protrusion in elasmobranchs. Journal of Morphology 222 175-190.

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115 Figure 2.1. Phylogeny of the hammerhead shar ks modified from Lim et al. (2010). Based on the nuclear genes ITS2, Dlx1, and Dlx2 and the mitochondrial genes NADH dehydrogenase 2, cytochrome b cytochrome oxidase I, and D-loop. Differences in head shape among the species are indi cated with non scaled line dr awings of the cephalofoil. Body size differences are shown among the speci es with a generalize d body shape scaled to maximum reported size for each species. Numbers above the nodes are posterior probabilities and numbers below the node are BE ST credibility values. Numbers to the right of the nodes indicate nodes for ancestral state reconstructions. Head shapes and body outlines modified from Compagno, 1984. Scale bar = 1 m.

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116 Figure 2.2. Dorsal (a) and lateral (b) views of the cartilaginous elements within the cephalofoil of S. lewini Chondrocranium – light gree n, Palatoquadrate – light blue, Meckel’s cartilage – dark blue, Hyomandi bula – pink, Ceratohyal – purple, and Basihyal – dark green

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117 Figure 2.3. Morphology of the feeding a pparatus shown on a reconstruction of S. lewini The four principal jaw closing muscles, QMD – quadratomandibul aris dorsal, QMV – quadratomandibularis ventral, POD – preorbitalis dorsal, an d POV – preorbitalis ventral are overlain on the reconstruction. The left nasal capsule and optic cartilages have been trimmed to reveal the origin of POV on the nasal capsule.

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118 Figure 2.4. PCA plot of TL removed raw feed ing morphology data. PC1 explained 49.7% of the variation and indicates increasing values of anterior bite force, posterior bite force, QMV and QMD mass, and QMV a nd QMD force. While PC2 explained 27.2% of the variation and indicates increasing values of POV and POD mass and for ce. Generalized head shapes have been added to indica te where each shape lies within multivariate spac e (head shapes modified from Compagno, 1984).

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119 Figure 2.5. Chondrocranium, mandibular, an d hyoid arch skeletons of each species overlain onto phylogeny. Phylogeny simplif ied from Lim et al., 2010. Numbers represent ancestral character state rec onstruction nodes. Scale bars = 5 cm.

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120 Figure 2.6. Raw bite force among sphyr nid and closely related carcharhinid species. Small bodied species ( E. blochii S. tudes and S. tiburo ) clearly group together as do large bodied species ( S. mokarran S. zygaena and S. lewini ). Furthermore, E. blochii (green dots), S. zygaena (orange dots), S. tiburo (black dots) have anterior bite force values that are lower than predicted.

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121Table 2.1. Average raw values s.e. for feeding mor phology variables for sphyrnid and carcharhinid species. TL (cm) Head Width (cm) Weighted InLever (cm) Anterior Outlever (cm) Posterior Outlever (cm) AMA PMA C. acronotus 102.6 2.52 11.43 0.26 2.38 0.089 7.26 0.22 2.02 0.055 0.33 0.0037 1.18 0.025 R. terraenovae 88.36 1.35 9.14 0.072 2.00 0.089 6.71 0.11 1.70 0.056 0.30 0.01 1.18 0.045 E. blochii 132.18 10.07 53.24 3.52 2.02 0.27 7.76 0.77 2.15 0.21 0.26 0.015 0.93 0.048 S. mokarran 286.14 34.16 67.18 9.11 5.33 0.81 20.41 3.38 6.43 1.14 0.26 0.011 0.84 0.031 S. zygaena 262.50 30.50 68.00 8.00 3.77 0.29 16.26 1.85 3.79 0.59 0.12 0.098 1.01 0.08 S. lewini 257.14 3.34 60.18 1.16 3.41 0.14 14.56 0.58 4.52 0.32 0.24 0.014 0.76 0.036 S. tudes 92.52 4.92 21.34 3.10 1.41 0.063 6.04 0.34 1.64 0.14 0.24 0.012 0.88 0.061 S. tiburo 88.10 1.17 13.66 0.23 1.25 0.068 5.76 0.10 1.51 0.087 0.22 0.013 0.84 0.072 Phylogenetically corrected size-removed data showed head width had no aff ect on any feeding morphology variable.

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122Table 2.1 Continued. Average raw values s.e. for feeding morphology variables fo r sphyrnid and carcharhinid species. TL (cm) ABF (N) PBF (N) QMV Force (N) QMD Force (N) POV Force (N) POD Force (N) C. acronotus 102.60 2.52 67.02 7.97 270.05 33.77 108.55 8.45 48.41 5.36 37.25 4.32 12.31 1.12 R. terraenovae 88.36 1.35 38.59 2.57 157.68 7.94 80.17 3.94 33.49 1.37 11.24 1.21 8.61 0.78 E. blochii 132.18 10.07 52.11 8.31 171.77 30.56 83.49 19.43 36.50 6.84 52.22 11.86 32.86 7.06 S. mokarran 286.14 34.16 642.22 260.34 1839.43 720.05 821.77 268.63 574.42 212.44 341.83 138.51 234.93 96.54 S. zygaena 262.50 30.50 288.49 47.00 1210.00 128.00 372.16 78.54 252.30 34.39 209.60 26.29 93.06 26.73 S. lewini 257.14 3.34 207.4 23.20 623.05 23.82 244.76 17.02 161.58 9.56 168.75 7.50 100.23 4.67 S. tudes 92.52 4.92 38.36 6.19 139.04 21.10 59.85 7.94 25.84 3.88 40.72 6.55 19.65 3.08 S. tiburo 88.10 1.17 18.2 2.09 71.08 6.05 36.16 2.44 17.05 1.02 29.54 1.96 18.41 0.95 Phylogenetically corrected size-removed data showed head width had no affect on a ny feeding morphology variable. N = Newtons

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123Table 2.1 Continued. Average raw values s.e. for feeding morphology variables for sphyrnid and carch arhinid species. TL (cm) QMV Mass (g) QMD Mass (g) POV Mass (g) POD Mass (g) C. acronotus 102.6 2.52 8.88 0.80 5.14 0.51 5.3 0.51 1.8 0.15 R. terraenovae 88.36 1.35 4.72 0.30 2.64 0.29 1.48 0.058 0.74 0.068 E. blochii 132.18 10.07 5.11 1.50 3.3 0.94 5.78 1.70 3.47 1.03 S. mokarran 286.14 34.16 198.22 114.27 99.12 57.76 141.76 80.44 82.58 47.34 S. zygaena 262.5 30.5 49.80 18.10 25.75 9.75 48.00 17.20 22.55 8.05 S. lewini 257.14 3.34 29.6 1.83 20.73 1.46 39.92 1.69 20.18 1.77 S. tudes 92.52 4.92 2.54 0.37 1.82 0.33 5.12 0.84 2.04 0.35 S. tiburo 88.1 1.17 1.58 0.058 1.04 0.87 2.64 0.14 1.58 0.11 Phylogenetically corrected size-removed data showed head width had no aff ect on any feeding morphology variable.

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124Table 2.2. Average raw volumes (cm3) s.e. for the cartilaginous el ements of the feeding system of sphyrnid and carcharhinid species. TL (cm)Palatoquadrate Meckel’s Cartilage Hyomandibula Ceratohyal Basihyal Chondrocranium C. acronotus 102.6 2.52 11.15 1.55 14.65 1.84 4.33 0.66 6.15 0.75 2.19 0.24 61.94 6.70 R. terraenovae 88.36 1.35 5.19 0.18 7.05 0.71 1.97 0.10 2.43 0.15 1.17 0.13 31.80 1.83 E. blochii 132.18 10.07 11.43 2.00 15.50 3.15 6.71 1.12 4.77 0.45 1.91 0.092 161.07 22.47 S. mokarran 286.14 34.16 73.57 11.61 101.43 17.18 34.69 6.26 20.35 2.98 7.06 1.06 512.17 81.21 S. zygaena 262.5 30.5 32.56 9.95 45.03 13.28 19.95 6.95 14.58 5.22 10.00 2.83 677.35 195.70 S. lewini 257.14 3.34 55.34 11.25 69.86 12.43 26.06 6.95 19.88 3.95 10.04 1.61 571.17 27.42 S. tudes 92.52 4.92 2.22 0.53 2.96 0.67 1.34 0.31 0.98 0.23 1.11 0.26 41.99 7.37 S. tiburo 88.1 1.17 4.45 0.34 5.49 0.45 2.18 0.10 1.59 0.029 0.61 0.073 24.53 1.77 The volumes of the palatoquadrate, Meckel’s cartilage, hy omandibula, and ceratohyal were all positively correlated through phylogeny (p < 0.05).

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125 Table 2.3. Percent contribution of each mu scle to total force production among sphyrnid and carcharhinid species. Average TL (cm) QMV QMD POV*,** POD** Total Force Produced by Muscles (N) C. acronotus 102.6 2.52 52.56 23.44 18.04 5.96 206.52 R. terraenovae 88.36 1.35 60.05 25.08 8.42 6.45 133.51 E. blochii 132.18 10.07 40.71 17.80 25.46 16.02 205.07 S. mokarran 286.14 34.16 41.65 29.11 17.33 11.91 1972.95 S. zygaena 262.5 30.5 39.82 26.34 23.35 10.49 730.45 S. lewini 257.14 3.34 36.24 23.93 24.99 14.84 675.32 S. tudes 92.52 4.92 40.98 17.69 27.88 13.45 146.06 S. tiburo 88.1 1.17 35.75 16.85 29.20 18.20 101.16 Multiple linear regression indicated that the be st predictor of anterior bite force was POV force (* p = 0.029). Similarly, the best pred ictor of posterior bite force was POV and POD force (** p < 0.001) along with posterior mechanical advantage. N = Newtons

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126 Table 2.4. Bite force among sphyrnid and outgroup carcharhinid species. Species TL (cm) Anterior Bite Force (N) Residual Bite Force Average Residual Bite Force C. acronotus 93.5 107.5 56.62 91.69 0.23 1.76 1.18 R. terraenovae 85 92.6 30.25 46.01 -0.0047 1.25 0.66 E. blochii 109 165.6 30.73 80.24 -1.22 -0.24 -0.77 S. mokarran 210 399 193.42 1630 0.07 2.06 0.87 S. zygaena 246.4 265.5 154.87 193.83 -0.77 -1.74 -1.26 S. lewini 232 293 188.18 335.48 -1.05 0.095 -0.44 S. tudes 73.5 102 14.67 51.04 -0.75 0.99 0.25 S. tiburo 85 91.5 13.41 25.62 -1.73 -0.52 -1.22 Ranges for anterior bite force and size-rem oved residual bite force and overall average residual bite force for each species. Anteri or bite force and shark TL were first log10 transformed and then regressed against one another (Log ABF = 2.144(Log TL) – 2.705).

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127 Table 2.5. Correlation matrix of feeding and head morphology data for sphyrnid and carcharhinid species. AMA PMA ABF PBF QMV Mass QMD Mass POV Mass POD Mass QMV Force QMD Force POV Force POD Force Head Width (cm) -0.11-0.250.46 -0.14-0.21-0.16-0.100.21 -0.47 -0.16 0.36 0.45 0.42 0.31 0.18 0.39 0.34 0.38 0.43 0.35 0.18 0.38 0.24 0.19 QMV (cm3) 0.63 -0.16-0.19-0.570.45 0.47 -0.180.12 0.68 0.29 -0.32 0.03 0.09 0.38 0.36 0.12 0.19 0.18 0.36 0.41 0.07 0.29 0.27 0.48 QMD (cm3) 0.69 -0.350.02 -0.650.56 0.65 -0.020.29 0.60 0.39 -0.16 0.19 0.07 0.25 0.48 0.08 0.12 0.08 0.49 0.29 0.11 0.22 0.38 0.36 POV (cm3) 0.76 -0.55-0.10 -0.81 0.34 0.45 0.13 0.30 0.55 0.22 -0.10 0.28 0.04 0.13 0.43 0.03 0.25 0.18 0.40 0.28 0.13 0.34 0.42 0.29 POD (cm3) 0.70 -0.610.10 -0.77 0.52 0.60 0.22 0.52 0.61 0.42 0.11 0.49 0.06 0.10 0.42 0.04 0.14 0.10 0.34 0.15 0.10 0.20 0.42 0.16 Eye (cm3) 0.27 -0.210.41 -0.15 0.77 0.88 0.29 0.43 0.33 0.66 0.15 0.21 0.30 0.35 0.21 0.39 0.04 0.01 0.29 0.20 0.26 0.08 0.39 0.35 Nasal Capsule (cm3) 0.40 -0.390.50 -0.42 0.85 0.85 0.11 0.71 0.59 0.77 0.33 0.63 0.22 0.23 0.16 0.20 0.02 0.02 0.42 0.06 0.11 0.04 0.26 0.09 Olfactory Tract (cm3) 0.81 -0.66-0.13 -0.95 -0.110.09 0.03 0.11 0.10 -0.23 -0.16 0.24 0.03 0.08 0.40 0.00 0.42 0.43 0.48 0.42 0.43 0.33 0.38 0.32 Braincase (cm3) 0.16 0.09 -0.70-0.17 -0.86-0.74 -0.19-0.73-0.39 -0.87 -0.59 -0.61 0.38 0.44 0.06 0.38 0.02 0.05 0.36 0.05 0.22 0.01 0.11 0.10 Palatoquadrate (cm3) 0.75 -0.440.02 -0.74 0.49 0.62 0.04 0.30 0.53 0.33 -0.14 0.23 0.05 0.19 0.48 0.05 0.16 0.10 0.47 0.28 0.14 0.26 0.39 0.33 Meckel’s Cartilage (cm3) 0.76 -0.42-0.06 -0.75 0.42 0.54 -0.010.24 0.54 0.26 -0.21 0.17 0.04 0.21 0.46 0.04 0.20 0.13 0.50 0.33 0.14 0.31 0.35 0.37 Hyomandibula (cm3) 0.76 -0.44-0.10 -0.78 0.38 0.47 -0.020.24 0.57 0.23 -0.19 0.21 0.04 0.19 0.42 0.04 0.23 0.17 0.49 0.32 0.12 0.33 0.36 0.35 Ceratohyal (cm3) 0.59 -0.05-0.03-0.440.40 0.54 -0.25-0.040.29 0.19 -0.43 -0.18 0.11 0.47 0.48 0.19 0.22 0.14 0.32 0.47 0.29 0.36 0.20 0.37 Basihyal (cm3) 0.04 0.25 -0.66-0.01 -0.89-0.78 -0.30 -0.83 -0.53 -0.92 -0.64 -0.73 0.47 0.32 0.08 0.50 0.01 0.03 0.28 0.02 0.14 0.01 0.08 0.05 Chondrocranium (cm3) 0.07 0.21 -0.68-0.07 -0.96-0.89 -0.36 -0.81 -0.53 -0.97 -0.61 -0.64 0.45 0.34 0.07 0.45 0.00 0.01 0.24 0.03 0.14 0.00 0.10 0.09 Total Volume (cm3) 0.09 0.16 -0.69-0.08 -0.86-0.75 -0.21 -0.77 -0.43 -0.87 -0.61 -0.67 0.43 0.38 0.06 0.44 0.01 0.04 0.35 0.04 0.20 0.01 0.10 0.07 Dorsal Pore Count (#) 0.40 -0.32-0.14-0.48 -0.77 -0.50-0.10-0.39 -0.82 -0.81 -0.26 -0.16 0.21 0.27 0.40 0.17 0.04 0.16 0.43 0.22 0.02 0.03 0.31 0.38 Ventral Pore Count (#) 0.50 -0.33-0.17-0.56-0.56-0.22-0.06-0.40-0.60 -0.68 -0.41 -0.28 0.16 0.26 0.37 0.12 0.12 0.34 0.46 0.22 0.10 0.07 0.21 0.29 AMA 1.00 -0.49-0.21 -0.90 -0.010.20 -0.07-0.020.06 -0.18 -0.36 0.02 0.16 0.34 0.01 0.49 0.35 0.45 0.48 0.46 0.37 0.24 0.48 PMA 1.00 -0.47 0.74 -0.18-0.44-0.71-0.660.07 -0.18 -0.55 -0.75 . 0.18 0.05 0.37 0.19 0.06 0.08 0.45 0.37 0.13 0.04 ABF (N) . 1.00 -0.020.58 0.70 0.47 0.79 -0.13 0.62 0.80 0.78 . 0.49 0.11 0.06 0.17 0.03 0.41 0.10 0.03 0.03 PBF (N) . 1.00 0.01 -0.25-0.11-0.20-0.01 0.14 0.09 -0.32 . . 0.49 0.32 0.42 0.35 0.50 0.40 0.43 0.27 QMV Mass (g) . . 1.00 0.92 0.29 0.76 0.66 0.97 0.49 0.56 . . 0.01 0.29 0.04 0.08 0.00 0.16 0.12 QMD Mass (g) . . 1.00 0.42 0.78 0.43 0.86 0.50 0.62 . . . 0.21 0.03 0.20 0.02 0.16 0.09 POV Mass (g) . . . 1.00 0.70 0.04 0.41 0.78 0.65 . . . 0.06 0.47 0.21 0.03 0.08 POD Mass (g) . . . 1.00 0.36 0.82 0.89 0.96 . . . . 0.24 0.02 0.01 0.00 QMV Force (N) . . . . 1.00 0.66 0.07 0.21 . . . . 0.08 0.45 0.35 QMD Force (N) . . . . 1.00 0.64 0.64 . . . . . 0.09 0.09 POV Force (N) . . . . . 1.00 0.89 . . . . . 0.01 Correlation coefficients are indicated in the top line of a structure and the p-value is in the second. Blue = positive correlations while re d = negative correlations. N = Newtons

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128 Table 2.6. Ancestral state reconstructions at each of the nodes along phylogeny (Figure 1). Basal Derived Node 2 3 4 7 5 6 Head Width (cm) 37.89 46.64 46.40 51.48 37.59 22.63 TL (cm) 164.92 179.08 185.79 206.20 164.77 113.01 QMV Volume (cm3) 21.03 22.09 23.41 30.89 15.61 5.32 QMD Volume (cm3) 13.32 14.00 14.78 18.42 10.89 4.09 POV Volume (cm3) 21.74 25.15 26.81 32.74 21.01 8.88 POD Volume (cm3) 10.89 13.39 14.16 17.20 10.99 4.56 Palatoquadrate Volume (cm3) 17.24 18.66 19.78 24.52 14.87 5.47 Meckel’s cartilage Volume (cm3) 23.00 24.94 26.43 33.08 19.49 7.09 Hyomandibula Volume (cm3) 8.88 10.10 10.63 13.27 7.77 2.94 Ceratohyal Volume (cm3) 7.10 7.30 7.65 9.38 5.73 2.16 Basihyal Volume (cm3) 3.48 3.79 4.09 5.05 3.22 1.36 AMA 0.20 0.18 0.17 0.15 0.20 0.21 PMA 0.93 0.89 0.89 0.90 0.85 0.85 ABF (N) 108.06 117.96 129.84 171.76 93.48 41.52 PBF (N) 387.61 414.85 459.69 616.27 327.36 153.11 QMV Mass (g) 13.65 14.75 16.90 24.80 10.87 3.74 QMD Mass (g) 8.15 8.86 10.05 14.08 6.91 2.47 POV Mass (g) 14.07 16.72 19.25 26.17 14.50 6.08 POD Mass (g) 6.87 8.68 9.86 13.37 7.26 2.96 QMV Force (N) 157.69 168.56 184.32 238.91 136.04 68.77 QMD Force (N) 85.59 94.87 106.26 144.21 75.66 33.50 POV Force (N) 85.06 98.63 107.56 132.30 87.27 48.02 POD Force (N) 43.90 54.85 59.10 71.19 48.63 26.42 Reconstructions indicate that the closest relative between sphyrnid and carcharhinid sharks was a relatively large bodied ( 163.21 cm TL), with a moderately expanded cephalofoil (~23% of TL), numbers of both dorsal and ventral por es consistent with extant sphyrnids, anterior and posterior bite force values of 108.1 N and 387.6 N respectively, with the QMV contributing ~ 43% of the total force produced by the feeding muscles. N = Newtons

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129 CHAPTER 3: BITE FORCE AND PERFORMANCE IN THE DUROPHAGOUS BONNETHEAD SHARK, SPHYRNA TIBURO ABSTRACT Bite force, a measure of performance, can be used to link anatomical form and function. Prior studies have shown bite force to have a significant influence on dietary constraints and ontogenetic shifts in resource utilization. The bonnethead shark, Sphyrna tiburo is a durophagous member of the family S phyrnidae. Its diet in south Florida waters consists almost entirely of blue crabs, which are crushed or i ngested whole. This abundant coastal predator’s f eeding mechanism is specialized for the consumption of hard prey, including a modified biting pattern and molariform teeth. The goals of this research were to: 1) characterize the mechan ical function of the feeding mechanism of S. tiburo through biomechanical modeling of biting and in vivo bite force measurements; 2) compare the bite force of S. tiburo with those of other fishes ; and 3) identify functional constraints on prey capture by comparing the bite force of S. tiburo to the fracture properties of its primary prey item, blue cr abs. Maximum theoretical bite force ranged from 25.7 N anteriorly to 107.9 N posteriorly. Sphyrna tiburo has the second lowest mass specific bite force for any fish studie d to date, and its posterior mechanical advantage of 0.88 is lower than other duropha gous chondrichthyans, indicating that this independent evolutionary acquisition of durophagy was not accompanied by the associated morphological changes found in othe r durophagous cartilaginous fishes. Blue

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130 crab fracture forces (30.0-490.0 N) range well above the maximum bite force of S. tiburo suggesting that prey material properties func tionally constrain dietary ecology to some degree. INTRODUCTION While the relationship between form and function is often times apparent, a key component to understanding the relationship between these parameters and ecology is performance, the ability of an organism to accomplish ecologically relevant tasks (Arnold, 1983; Irschick, 2002). More so, to dr aw substantive conclu sions regarding such relationships both within and am ong species, these data must be investigated in light of the functional constraints im posed by ecological tasks. Doing so has elucidated numerous correlations between morphology and va riables such as prey type, habitat, and community structure (Herrel et al., 1996; Irschick and Losos, 1999; Korff and Wainwright, 2004; Toro et al., 2004). Bite for ce influences the ability to acquire food resources, and has thus been an extensivel y studied performance measure in vertebrates (fish (Wainwright, 1988; Herrel et al., 2002a; Korff and Wain wright, 2004; Grubich, 2005; Huber et al., 2005; 2009; Kolmann and H uber, 2009), lizards (Herrel et al., 2001a; Lailvaux and Irschick, 2007), croc odilians (Erickson et al., 2003) birds (van der Meij and Bout, 2000; 2006; Herrel et al., 2005a; b), a nd mammals (Kiltie, 1982; Aguirre et al., 2003; Herrel et al., 2008)). Although bite forces are informative regard ing the relative and absolute abilities of animals to capture and process prey, ecol ogical conclusions drawn from these data are suspect without specific attention paid to th e functional constraints imposed by these prey

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131 items. For durophagous species (consumers of ha rd prey), bite force is particularly influential in shaping diet be cause the exoskeletal armaments of their prey are among the most durable biological materials found in th e aquatic environment (Wainwright et al., 1976; Summers and Long Jr ., 2006). Despite the diversity of bite force studies, few have related bite force to prey characteristics in fish (Wainwright, 1988; Hernndez and Motta, 1997; Korff and Wainwri ght, 2004; Grubich, 2005), with only a single study investigating this in cartilaginous fishes (Kolmann and Huber, 2009). The feeding mechanisms of chondrichthyans are remarkably different from those of bony fishes. They lack pharyngeal jaws to further process prey and have skeletons composed of prismatically calcified cartilage. Despite having jaws primarily composed of a pliant skeletal material, durophagy has conv ergently evolved at least eight times in groups such as the heterodontids, orectolobi ds, triakids, sphyrnids, and chimaeroids (Compagno et al., 2005; Huber et al., 2005; Ramsay and Wilga, 2007; Huber et al., 2008). Durophagy in chondrichthyan fishes is often associated with hypertrophy of their jaws and adductor muscles, molariform teeth, high bite force, and fused jaw symphyses in some cases (Summers, 2000; Summers et al., 2004; Huber et al., 2005). Behavioral and functional modifications associated with hard prey consumption also include unilateral biting and asynchronous muscle ac tivity (Summers, 2000), tooth reorientation during biting (Ramsay and Wilga, 2007), an d specialized motor patterns (Summers, 2000; Wilga and Motta, 2000). Collectively thes e characteristics are often related to dietary specialization ( Rhinoptera bonasus Summers, 2000; Sa sko et al., 2006; Heterodontus francisci Huber et al., 2005; Sphyrna tiburo Corts et al., 1996).

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132 The bonnethead shark, Sphyrna tiburo (Elasmobranchii, Sphyrnidae) is purportedly the most derived hammerhead species (Martin, 1993; Martin and Palumbi, 1993), specializing almost exclusively on crus tacean prey, particularly swimming crabs ( Callinectes sp.) in south Florida (Compagno, 1984; Corts et al., 1996; Lessa and Almeida, 1998; Bethea et al., 2007). Compar ed to other sharks, the bonnethead shark exhibits less upper jaw prot rusion, prolonged jaw adductor ac tivity patterns, enlarged maximum gape, and is the only hammerhead shark with posterior molariform teeth (Wilga and Motta, 2000; Motta and W ilga, 2001). However, durophagy in S. tiburo is enigmatic in that it is accomplished with so me, but not all, of the characteristics associated with durophagy in other chondrichthya ns. In particular, they lack robust jaws, hypertrophied feeding muscles, and fused jaw symphyses (Wilga and Motta, 2000). However, relatively little is known about how feeding morphology contributes to force generation and shapes not only diet but also feeding ecology in S. tiburo The goals of this study were therefore to: 1) characteri ze the mechanical function of the feeding mechanism of S. tiburo through biomechanical modeling of biting and bite force measurements obtained via tetanic stimulation of jaw muscles and restraint of live animals; 2) compare the bite force of S. tiburo with that of other fishes; and 3) identify functional constraints on pr ey capture and diet by comparing the bite force of S. tiburo to the fracture properties of its pr imary prey item, blue crabs.

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133 MATERIALS AND METHODS Experimental Animals Ten Sphyrna tiburo (55.2 68.7 cm precaudal le ngth (PCL), 73.0 91.5 cm total length (TL), 1644 3420 g) were collected from the Gulf of Mexico off Sarasota, Florida using a combination of long-li ne and gill net fishing. Shar ks were chosen within a narrow size range to remove the effect of ontogeny. For ease of comparison to dietary data (Corts et al., 1996) shark PCL is used throughout. Individuals were housed in a 9.1 x 16.8 x 1.8 m., 22.7 kl oval tank located at Mote Ma rine Laboratory in Sarasota, Florida. Animals were fed bi-weekly with a diet of threadfin herring ( Opisthonema oglinum ) and white shrimp ( Penaeus setiferus ) as attempts to feed S. tiburo blue crabs in captivity were unsuccessful. However, cranial muscle plas ticity data for elasmobranchs is lacking, therefore the potential effects of diet on muscle atr ophy are unknown. In south Florida, the index of relative importance (IRI) (Pinka s et al., 1971) indicates that the diet of S. tiburo is dominated by blue crab, Callinectes sapidus (85%). Within the size range of shark studied here, the occurrence of C. sapidus in the diet increases to 90% with the remaining diet being seagrass, most likely in cidentally ingested (Corts et al., 1996). Upon completion of in vivo force measurements all animals were euthanized with an overdose of tricaine methanesulphonate (MS-222 0.1 g/L). All experimental procedures followed the Institutional Animal Care and Use Committee guidelines of Mote Marine Laboratory (08-10-RH1, 07-10-PM 1) and the University of South Florida (T3198, R3205, W3514).

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134 Theoretical Bite Force The three-dimensional coordinates of th e origins and insertions for the four principal muscles involved in jaw adduction (preorbitalis dorsal (POD), preorbitalis ventral (POV), quadratomandibularis dorsal (QMD), and quadratomandibularis ventral (QMV)) (Wilga and Motta, 2000) (Figure 3.1), the jaw joint, and anterior and posterior bite points along the lower jaw were obtained using a three-dimensi onal Patriot digitizer (Polhemus, Colchester, VT, USA) with the ti p of the rostrum as the center of a threedimensional coordinate system. Followi ng Huber et al. (2005), each muscle was unilaterally excised and the center of mass was determined. Center of mass and the superficial muscle fiber architecture were then used to estimate the line of action of each muscle, from which muscle origins and insertions were determined. The in-lever for each muscle was calculated based on the coordinates of its insertion on the lower jaw and the jaw joint. A resolved in-lever for jaw adduc tion was then determin ed from a weighted average of these individual in-levers based on the proportion of force that each muscle contributed to overall force produ ction. Out-lever distances to the anterior and posterior bite points were determined from the coordina tes of the anterior a nd posterior margins of the functional tooth row and the jaw joint. Mechanical advantage for jaw adduction at the anterior and posterior bite points was then calculated by dividing the weighted inlever by the respective out-lever (Huber et al., 2006; 2008). It is assumed that all skeletal elements act as rigid beams and mechanical a dvantage is equivalent to ideal mechanical advantage in this system. The mechanical advantage of a jaw adducting system indicates the ability of the system to transfer muscle fo rces to prey either rapidly (low mechanical advantage) or forcefully (high m echanical advantage) (Westneat, 2003).

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135 Following excision, each muscle was bisected perpendicular to the principal fiber direction through the cente r of mass and the cross sectional area was digitized with Sigma Scan Pro 4 (SYSTAT Software Inc., Point Richmond, CA, USA) (Hub er et al., 2005). Maximum tetanic tension for each muscle was calculated by multiplying the cross sectional area by the specific tension of elasmobranch white muscle (28.9 N/cm2, Lou et al., 2002). Forces and positions were then used to create three-dimensional force vectors for each muscle. Bilateral theoretical maximum bite force at anterior and posterior bite points was modeled in 3D with Mathcad 13 (Mathsoft, Inc., Cambridge, MA, USA) by summation of the moments generated about the jaw join ts by each muscle (Huber et al., 2005). The static equilibrium model for lower jaw adduction is: 0 F F F F F F F B JR QV QD PV PD LJ, where FPD is the force contributed by the preorbitalis dorsal, FPV is the force contributed by the preorbitalis ventral, FQD is the force contributed by the quadratomandibularis dorsal, FQV is the force contributed by the quadratomandibularis ventral, FJR is the joint reaction force, and FB is the reaction force from the prey. Restrained Bite Force Previous studies have demonstrated that theoretical modeling of bite force in chondrichthyans is a good proxy for in vivo maximum biting performance (Huber et al., 2005). However, no study has investigated the predictive power of theoretical bite force calculations in a species with morphological di vergence in head shape. The collection of in vivo data allows for verification of the theoretical model. All in vivo bite force measurements were collected with a modifi ed single-point load cell (AmCells Corp.,

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136 Vista, CA, USA) which was calibrated using a digital scale (Siltec Scales, Santa Clara, CA, USA). The transducer was connected to a P-3500 strain indicator (Vishay Measurements Group, Raleigh, NC USA). Data were sent to a 6020E data acquisition board and imported into LabVIEW 6.0 software (National Instruments Corp., Austin, TX, USA). Individual animals were removed from the holding tank and restrained on a foam padded platform such that thei r head hung over the edge of th e platform. The tip of the rostrum was elevated and the metal arms of the transducer were placed between the anterior tips of the jaws eliciting a bite. The anterior placement of the force transducer was chosen because it cannot be placed farthe r back due to gape constraints. This procedure was repeated 3-5 times for each i ndividual and the largest of the 3-5 values was recorded as the maximum bite force for that individual. The procedure took no longer than 5 minutes per individual. Tetanic Bite Force Following restrained bite force measurements, the sharks were anesthetized with a re-circulating, aerated solution of MS-222 (0.133g l-1) and seawater. Once fully anesthetized, the sharks were placed vent ral side up in a holding apparatus and the preorbitalis ventral, quadratomandibularis dorsal, and quadratom andibularis ventral muscles were implanted with bipolar electrodes connected to a SD9 stimulator (Grass Instruments, Quincy, MA, USA.). The preorb italis dorsal was not stimulated because its small size and location made it difficult to implant. The jaw muscles were tetanically stimulated with the bite force transducer placed between the anterior tips of the jaws (20 V, 100Hz, 0.02 ms delay, 3ms pulse duration). Each individual was stimulated 3-4 times with a minimum of 1-2 minutes between su ccessive stimulation events, during which

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137 their gills were perfused with the aerated anesth etic solution. The maximum force value for each individual was recorded. Posterior forces for all in vivo tests were calculated by multiplying the anterior force by the ratio of anterior to posterior out-levers. Performance Testing of Prey Eighteen live inter-molt C. sapidus (23.3 68.4 mm carapace length (CL)) representing the crabs greater than or equal to the size range consumed by the sample of sharks from this study (Corts et al., 1996) were purchased from local bait shops or collected by beach seine. The carapace width (spine to spine), length, depth, and mass were recorded for all C. sapidus prior to material testing. Upper and lower jaws were rem oved from an adult 78.4 cm PCL S. tiburo and dried in 95% ethanol for 12 hours in order to bond them to steel plates such that the occlusal surfaces of the teeth were aligned. Th e jaws of this individual are comparable to those of sharks from our sample size both in size and shape. The pl ates were mounted in a Mini Bionix II Material Testing System (MTS, Eden Prairie, MN, USA) with an in-line 5 kN load cell. Live crabs were immobilized with a combination of MS-222, ~0.1g/L, and tonic immobility (Fedotov et al., 2006), a nd placed between the mounted jaws. Live crabs are required for this type of experi ment because the mechanical properties of biomaterials can change postmortem (LaBarbera and Merz, 1992). Crabs were crushed at a displacement rate of ~370 mm /s, which is the average veloc ity of lower jaw elevation in S. tiburo (Mara and Motta unpublished data ). In order to ensure m echanical failure of the carapace, the displacement dist ance was adjusted to 33% cara pace depth for each crab. A successful crushing event was defined as a la rge crack produced in the carapace, with peak force occurring immediatel y prior to carapace failure.

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138 Statistical Analyses All bite force variables, muscle ma sses, muscle forces, and mechanical advantages were log10 transformed and linearly regressed against shark total length to examine the effect of size on bite force. Given the small size range of S. tiburo in this study, regressions showed no si ze effects, therefore, log10 transformed (non-residual) values were used for the remaining statistical tests. Paired t-tests were used to identify differences among bite forces measured from theoretical, in vivo restrained, and in vivo stimulated treatments. A forward stepwise multiple linear regression was also performed to examine which morphological traits best expl ained variation in anterior theoretical bite force. To gain an understanding of how the bite force of S. tiburo compares to that of other fishes, particularly durophagous ones, maximum bite forces and body masses were compiled from the literature for eighteen sp ecies (Hernndez and Motta, 1997; Clifton and Motta, 1998; Huber and Motta, 2004; Ko rff and Wainwright, 2004; Huber et al., 2005; 2006; 2008; 2009; Huber and Mara unpublishe d). Bite forces and body masses for all species were log10 transformed and linearly regressed to determine mass-specific bite force, which was compared among species. Failure forces obtained during perfor mance testing of prey were log10 transformed and linearly regressed against crab carapa ce width, length, depth, and mass to examine the scaling of prey properties. The slopes of the scaling relationships were compared to an isometric slope of 2 with respect to crab width, length, and depth, and 0.67 with respect to mass using a two-tailed t-test. All regressions and paired t-tests were

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139 performed in SigmaStat 3.1 (SYSTAT Softwa re Inc., Point Richmond, CA, USA) and ttests of scaling relationshi ps were performed manually. RESULTS Feeding Biomechanics and Bite Force Of the jaw adducting muscles, the larg est force was produced by the QMV (33.2 2 SE N), which represented approximately 35% of the adductive force, followed by POV (27.7 1.4 SE N), POD ( 17.9 1 SE N), and QMD (17.4 0.8 SE N) (Table 3.1, Figure 3.2). Mechanical advantage range d from 0.24 – (0.02 SE) – 0.88 (0.04 SE) between the anterior and posterior bite po ints. Based upon these adductive forces and leverage of the feeding mechanism, the range of theoretical bite force was (13.4 – 25.7 N) and (50.3 – 107.9 N) for anterior and posterior bite points respectively. Forward stepwise multiple linear regression performed on all biom echanical variables with respect to bite force retained only the force generated by the QMD as a significant predictor of theoretical bite force (p=0.025). All other va riables had no predictive power due to their non-significant relationship to theoretical bite force. Theoretical mean maximum bite force for anterior (20.0 1.4 SE N) and posterior (77.4 5 SE N) biting were gr eater than restrained anteri or (14.2 1.2 SE N, p=0.017) and posterior (53.1 5.2 SE N, p=0.014) bite force. Anterior (17.3 2.1 SE N) and posterior (64.6 8.3 SE N) stimulated bite forc e were not different fr om either theoretical or restrained bite forces (Table 3.2) Size-removed bite force comparis on among fishes indicated that S. tiburo has the second lowest mass-specific bite force of any fi sh studied to date irrespective of diet.

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140 Only Etmopterus lucifer (-1.18) and Etmopterus spinax (-2.47) have a lower massspecific bite force than S. tiburo (-1.16). Furthermore, th e absolute bite force of S. tiburo is among the lowest of any durophagous fish (Table 3.3). Performance Testing of Prey Carapace fracture trials of C. sapidus typically exhibited a st eady increase in force until crack propagation began, followed by material failure (Figure 3.3). Failure forces ranged from 30.0 – 490.0 N and exhibited li near relationships with all crab morphometrics (carapace length, width, depth, and crab mass) (Figure 3.4). Failure force scaled isometrically relative to carapace width and length, and with positive allometry relative to carapace depth and crab mass (T able 3.4). Deeper heavier crabs require disproportionally more force to frac ture than thinner lighter crabs. For ease of comparison to dietary data, th e scaling relationship of CL to failure force will be discussed furt her. The non log transformed linear relationship between CL and failure force (y=11.08x–308.08, p < 001, R2=0.95) was used to estimate the range of C. sapidus that sharks in this study are capable of crushing. Base d upon the range of maximum posterior bite force from the e xperimental analyses (50.3 N, 62.5 cm PCL107.9 N, 60.0 cm PCL), the largest blue crab that S. tiburo of 55.2-68.7 cm PCL are capable of crushing range between 32.3 mm CL (62.8 mm CW) and 37.5 mm CL (73.9 mm CW) (Figure 3.5)

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141 DISCUSSION Feeding Biomechanics and Bite Force The bonnethead shark Sphyrna tiburo differs from other durophagous chondrichthyan and teleost fishes by having relatively low b ite force and a lack of: robust jaws, hypertrophied feeding muscles, an d fused jaw symphysis (Summers, 2000; Summers et al., 2004; Huber et al., 2005) During closing, the lower jaw of Sphyrna tiburo acts as a third class lever system with rela tively high force efficiency at the back of the jaws (posterior mechanical advantage = 0.88). However, the mechanical advantage of the bonnethead shark is not particularly large as force amplifying second class lever systems, with mechanical advantages gr eater than 1.0, have been found in other durophagous fishes, including chondrichthyan ( H. francisci and H. colliei ) and teleost oral and pharyngeal jaws (black drum, Pogonia cromis and striped burrfish, Chilomycterus schoepfi ) (Korff and Wainwright, 2004; Huber et al., 2005; Grubich, 2005; Huber et al., 2008). In fact, even non-dur ophagous fishes, such as the euryphagous blacktip shark, Carcharhinus limbatus (post. MA=1.09), have jaw adducting mechanisms with posterior mechanical advantage exceed ing 1.0 (Huber et al., 2006). It should be noted that second class lever systems cause joint reaction forces to switch from compression to tension at the jaw joint resu lting in greater chance for dislocation (Huber et al., 2008). The anterior mechanical advantage of S. tibur o (0.24) is comparable to those of numerous teleosts possessing low to intermediate jaw leverage (wrasses (0.130.41) gray triggerfish Balistes capriscus (0.25-0.27)), and consid erably lower than those of other durophagous fishes (horn (0.51), ch imaera (0.68), parrotf ish (0.45-1.04), etc.) (Durie and Turingan, 2001; Wainwright et al., 2004; Westneat, 2004). Furthermore,

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142 when only durophagous chondric hthyans are considered, S. tiburo has lower anterior and posterior mechanical adva ntages (Figure 3.6). Mass-specific bite force measurements are an indicator of the relative feeding performance of vertebrates. Durophagous taxa, such as the striped burrfish, Chilomycterus schoepfi (1.92, Table 3.3), typically have high mass-specific bite forces owing to relatively hypertrophied jaw adducto rs and high mechanical advantage of the feeding mechanism (Korff and Wainwright, 2004). Although S. tiburo has an almost exclusively durophagous diet, it surprisingly has the third lowest mass-specific bite force (-1.16) of any fish that has been studied. This includes soft prey specialists such as the spiny dogfish Squalus acanthias and non durophagous piscivores such as the lemon shark Negaprion brevirostris and blacktip shark Carcharhinus limbatus (Table 3.3) (Huber and Motta, 2004; Huber et al., 2005; 2008). The mass-specific bite force for S. tiburo places it above Etmopterus lucifer and E. spinax both of which are deepwater lantern sharks whose diet consists of small fishes, squi d, and some crustaceans (Compagno et al., 2005). While mass-specific bite force allows fo r comparison of relative ability among species, comparison of absolute bite force permits ecological predictions to be made about diet. Forces required to crush prey must be generated independent of predator mass, and absolute bite force values determin e the ability to consume a particular prey item (Huber et al., 2008). When comparing am ong species of similar size, the absolute bite force of S. tiburo is comparable to soft prey specialists such as S. acanthias and an order of magnitude smaller than other durophagous species such as H. francisci (Table 3.3).

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143 Although S. tiburo consumes hard shelled prey, it does so in a manner that is biomechanically different than previously de scribed in chondrichthyans. Animals that specialize on fast, agile, and elusive prey have speed-efficient jaw closing systems with low mechanical advantages (Turingan et al ., 1995). Previous studies have shown a tradeoff between bite force and the ability to capture elusive prey (Herrel et al., 2002b). The bonnethead shark feeding mechanism a ppears to be a compromise between adductive speed and force. Furthermor e, the jaw adducting musculature in S. tiburo can be active in a cyclical manner which could ai d in fracturing prey e xoskeletons (Wilga and Motta, 2000). This shark captures small, elus ive blue crabs by ram feeding with a wide gape and fast jaw closure (Wilga and Motta, 20 00) yet is constrained to smaller crabs by its limited bite force (see below). Model Verification Numerous methods for measuring bite force have been employed (Anderson et al., 2008), although few have been quantita tively compared (Huber and Motta, 2004; Huber et al., 2005). Previous studies have shown some methods of recording bite force are accurate predictors of maximum tetanic bi te force, whereas others are less so (Huber et al., 2005; Herrel et al., 2008). In previous studies of elasm obranch bite force, it has been shown that, in some cases, theoretically determined bite force accurately predicts those produced during in vivo voluntary testing (Huber et al., 2005). Furthermore, in bats theoretical morphological models of bite fo rce accurately predict bite force capacity (Herrel et al., 2008). However, other factor s not accounted for in our model (e.g., inertial fluid forces, resistance of body tissues) may influence the accuracy of our theoretical predictions (see Van Wa ssenbergh et al., 2005).

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144 These data show that 55.2-68.7 cm PCL bonnethead sharks are capable of producing a maximum bite force of 107.9 N at th e posterior molariform teeth (Table 3.2). In bonnethead sharks no differences were f ound between restrained and stimulated or stimulated and theoretical testing conditions However, both ante rior and posterior theoretical bite forces (20.0N and 77.4 N respectively) were greater than re strained bite force (14.2 N and 53.1 N respec tively). Both theoretical and stimulated testing conditions remove behavioral motivation as a potential variable. However, during restrained biting the animal can choose to perform less than maximally. Behavioral motivation, or lack thereof, can result in less than maximal performance (Irschick, 2002). During testing it was noted that restrained testing conditions e licited a reluctant bite from S. tiburo; the animal’s teeth had to be prodded numerous times to elicit a bite. Furthermore, S. tiburo did not voluntarily bite the force transducer even when presented with food. These results are contra ry to that of the horn shark, H. francisci where the sharks vigorously bit the offered force gauge, and restrained bite force was the largest among the three testing conditions (Huber et al., 2005). In the bonnethead shark, theoretical and stimulated bite force appear to be good indicators of performance, whereas voluntary bite force, under the condition s utilized here, is under representative of its biting capabilities. Ecological Performance Although high bite force may f acilitate a larger range of potential prey, it is often associated with dietary specialization becau se increased performance allows exploitation of prey resources unavailable to other species or availabl e to only a small number of species (Hernndez and Motta, 1997; Berume n and Pratchett, 2008). Thus, access to

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145 durophagous prey via high bite force has been shown to potentially reduce interspecific competition in fishes (Wainwright, 1988; Gr ubich, 2005), lizards (Herrel et al., 2001b), and mammals (Christiansen and Wroe, 2007). That bite force can determine diet is well known (Herrel et al., 2001b; Aguirre et al., 2003; Korff and Wainwright, 2004; Grubich, 2005). However, few studies relate bite force to characteristics of known prey species (Herrel et al., 2001b; Aguirre et al., 2003; Kolmann and Huber, 2009). In south Florida the diet of S. tiburo consists of almost exclusively blue crabs and may represent specialization on pr ey that is unavailable to other non-durophagous species. However, ma ximum bite force imposes limits on the size of its preferred prey with the maxi mum size blue crab consumed by bonnethead sharks in the size range studied here to ~ 60.2 mm CL (Corts et al ., 1996). Blue crabs reportedly reach a maximum size of 88.0 mm CL, leaving the upper 32% of the blue crab population unutilized by S. tiburo of this size range (A tar and Seer, 2003). When dietary data are compared to maximum b ite force, 57/72 crabs (~79%) consumed by bonnethead sharks in the size range sampled here are able to be crushed indicating that the majority of crabs consumed by S. tiburo fall well below their performance limits (Figure 3.5). Therefore, these data indicate that S. tiburo may be selecting blue crabs, in part based on some metric of size that relates to their ability to crush and consume them. Crabs falling outside of thei r performance limits would require dismemberment prior to consumption by lateral head shaking or other manipulation (Wilga and Motta, 2000; Matott et al., 2005). This is supported by many blue crabs found in the stomachs of S. tiburo being dismembered (E. Corts personal communication; K.R. Mara personal observation). Behavior and pr ey properties could also he lp explain the discrepancy

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146 between performance and diet. Elec tromyography data suggests that S. tiburo is capable of cyclical activity in the jaw adducting mu sculature which could aid in fracturing the carapace (Wilga and Motta, 2000). However, no study has quantitatively investigated this cyclical activity. Furthe rmore, individual variation in failure force could partially explain the 21% of crabs in the diet falling above the crushing ability of S. tiburo Our results provide an upper estimate of the force S. tiburo must produce to crush blue crabs and further data is required to address th e roles behavioral a nd variation in prey properties play in durophagy in S. tiburo. Durophagy is often assumed to relate dire ctly to mechanical function, however an animal can maintain a durophagous diet with out extensive modification of the feeding apparatus. It is known that the gastric pH of elasmobranch s can reach values as low as 0.4 (Papastamatiou and Lowe, 2005; Papastam atiou et al., 2007). Furthermore, chitinolytic enzyme activity has been pr eviously demonstrated in elasmobranchs (Lindsay, 1984). If bonnethead sharks have si milar gastric pH values or chitinolytic enzymes, the hard shell of their prey can be broken down chemically by the stomach rather than mechanically by the feeding apparatus. In this instance durophagy is established through the means of physiological modifications rather than morphological modifications. The apparent correlation between bite fo rce and diet could al so be explained by gape and processing time limitations Independent of bite for ce, larger items may not be consumed because of the physical dimensions of the gape or because of the adductor muscles being stretched beyond their optimal range (Kiltie, 1982; De Schepper et al., 2008). Furthermore, many studies have demonstr ated an increase in processing time with

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147 increased prey size (Verwaijen et al., 2002). The increased proces sing times required to consume very large crabs could make these crabs less cost effective to consume than smaller crabs with lower processing times. In addition large blue crabs may generate large crushing forces relative to other crabs which could resu lt in serious injury to the cephalofoil, leading S. tiburo to avoid potentially dangerous large blue crabs (Schenk and Wainwright, 2001). However, the ability of S. tiburo to process large prey remains to be tested. CONCLUSIONS Sphyrna tiburo is unlike other du rophagous chondrichthyan species. It has relatively low bite force and lacks hypert rophy of the feeding muscles and jaws. Furthermore, its posterior mechanical advantage is considerably lower than other species. In fact, the manner in which S. tiburo consumes hard prey is biomechanically different than previously described in chondrichthyans When the bonnethead shark is compared to a broad range of chondricht hyan and teleost species, its mass specific bite force is the second lowest of any species studied to date in spite of its pre dominately durophagous diet. Bite force modeling is an accurate predictor of maximu m biting capacities in S. tiburo However, behavioral motivation was found to play a large role in in vivo bite force measurements. The bite force of S. tiburo constrains the size of its preferred prey, blue crabs that it can consume. However, crabs that are larger than the maximum crushable size are consumed by S. tiburo This independent evolution of durophagy without the morphological modifications seen in other durophagous taxa, indicates that

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148 durophagy can be accomplished in the absence of high mechanical advantage and high bite force. LITERATURE CITED Aguirre, L. F., Herrel, A., Va n Damme, R., and Matthysen, E. (2003). The implications of food hardness for diet in bats. Functional Ecology 17 201-212. Anderson, R. A., McBrayer, L. D., and Herrel, A. (2008). Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animals performance measure. Biological Journal of the Linnean Society 93 709-720. Atar, H. H. and Seer, S. (2003). Width/length-weight rell ationships of the blue crabs (Callinectes sapidus Rathbun 1896) populat ion living in beymelek lagoon lake. Turkish Journal of Veterinary And Animal Science 27 443-447. Berumen, M. L. and Pratchett, M. S. (2008). Trade-offs associated with dietary specialization in corallivorous butterflyfishes (Chaetodontidae: Chaetodon ). Behavioral Ecology and Sociobiology 62 989-994. Bethea, D. M., Hale, L., Carlson, J. K., Co rts, E., Manire, C. A., and Gelsleichter, J. (2007). Geographic and ontogenetic variatio n in the diet and daily ration of the bonnethead shark, Sphyrna tiburo from the eastern Gulf of Mexico. Marine Biology 152 1009-1020. Christiansen, P. and Wroe, S. (2007). Bite forces and e volutionary adaptations to feeding ecology in carnivores. Ecology 88 347-358. Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shar k species known to data. Part 2. Carcharhiniformes. FAO Fish. Synop.: (125) Vol. 4, Pt. 2. Clifton, K. B. and Motta, P. J. (1998). Feeding morphology, diet, and ecomorphological relationships among five Caribbean labrids (Teleostei, Labridae). Copeia 1998 953-966. Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shar k species known to data. Part 2. Carcharhiniformes. FAO Fish. Synop.: (125) Vol. 4, Pt. 2. Compagno, L. J. V., Dando, M., and Fowler, S. (2005). Sharks of the world. Princeton, NJ: Princeton University Press.

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149 Corts, E., Manire, C. A., and Hueter, R. E. (1996). Diet, feedin g habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo in southwest Florida. Bulletin of Marine Science 58 353-367. De Schepper, N., Van Wassenbe rgh, S., and Adriaens, D. (2008). Morphology of the jaw system in trichiurids: trade-o ffs between mouth closing and biting performance. Zoological Journal of the Linnean Society 152 717-736. Durie, C. J. and Turingan, R. G. (2001). Relationship between durophagy and feeding biomechanics in gr ay triggerfish, Balistes capriscus : intraspecific variation in ecological morphology. Florida Scientist 64 20-28. Erickson, G. M., Lappin, A. K., and Vliet, K. A. (2003). The ontogeny of bite-force performance in American alligator ( Alligator mississippiensis ). Journal of Zoology, London 260 317-327. Fedotov, V. P., Kholodkevitch, S. V., and Udalova, G. P. (2006). Cardiac activity of freshwater crayfish at wakefuln ess, rest, and "animal hypnosis.". Journal of Evolutionary Biochemistry and Physiology 42 49-59. Grubich, J. R. (2005). Disparity between feeding performance and predicted muscle strength in the pharyngeal musculature of black drum, Pogonias cromis (Sciaenidae). Environmental Biology of Fishes 74 261-272. Hernndez, L. P. and Motta, P. J. (1997). Trophic consequences of differential performance: ontogeny of oral jaw-cr ushing performance in the sheepshead, Archosargus probatocephalus (Teleostei, Sparidae). Journal of Zoology, London 243 737-756. Herrel, A., Cleuren, J., and De Vree, F. (1996). Kinematics of feeding in the lizard Agama stellio Journal of Experimental Biology 199 1727-1742. Herrel, A., De Grauw, E., and Lemos-Espinal, J. A. (2001a). Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology 290 101107. Herrel, A., Van Damme, R., Vanhooydonck, B., and De Vree, F. (2001b). The implications of bite performance for di et in two species of lacertid lizards. Canadian Journal of Zoology 79 662-670. Herrel, A., Adriaens, D., Verraes, W., and Aerts, P. (2002a). Bite performance in clariid fishes with hypertrophied jaw a dductors as deduced by bite modeling. Journal of Morphology 253 196-205. Herrel, A., O'Reilly, J. C., and Richmond, A. M. (2002b). Evolution of bite performance in turtles. Journal of Evolutionary Biology 15 1083-1094.

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150 Herrel, A., Podos, J., Huber, S. K., and Hendry, A. P. (2005a). Bite performance and morphology in a population of Darwin's finche s: implications for the evolution of beak shape. Functional Ecology 19 43-48. Herrel, A., Podos, J., Huber, S. K., and Hendry, A. P. (2005b). Evolution of bite force in Darwin's finches: a ke y role for head width. Journal of Evolutionary Biology 18 669-675. Herrel, A., De Smet, A., Aguirre, L. F., and Aerts, P. (2008). Morphological and mechanical determinants of bite force in bats: do muscles matter? Journal of Experimental Biology 211 86-91. Huber, D. R. and Motta, P. J. (2004). Comparative analysis of methods for determining bite force in the spiny dogfish Squalus acanthias Journal of Experimental Zoology 301A 26-37. Huber, D. R., Eason, T. G., Hueter, R. E., and Motta, P. J. (2005). Analysis of the bite force and mechanical design of the f eeding mechanism of the durophagous horn shark Heterodontus francisci Journal of Experimental Biology 208 3553-3571. Huber, D. R., Weggelaar, C. L., and Motta, P. J. (2006). Scaling of bite force in the blacktip shark Carcharhinus limbatus Zoology 109 109-119. Huber, D. R., Dean, M. N., and Summers, A. P. (2008). Hard prey, soft jaws and the ontogeny of feeding mechanics in the spotted ratfish, Hydrolagus colliei Journal of the Royal Society Interface 5 941-952. Huber, D. R., Claes, J. M., Mallefet, J., and Herrel, A. (2009). Is extreme bite performance associated with ex treme morphologies in sharks? Physiological and Biochemical Zoology 82 20-28. Irschick, D. J. (2002). Evolutionary approaches for studying functional morphology: examples from studies of performance capacity. Integrative and Comparative Biology 42 278-290. Irschick, D. J. and Losos, J. B. (1999). Do Lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean Anoles. The American Naturalist 154, 293-305. Kiltie, R. A. (1982). Bite force as a basis for niche differentiation between rain forest peccaries ( Tayassu tajacu and T. pecari ). Biotropica 14 188-195. Kolmann, M. A. and Huber, D. R. (2009). Scaling of feeding biomechanics in the horn shark Heterodontus francisci : Ontogenetic constraints on durophagy. Zoology 112 351-361.

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151 Korff, W. L. and Wainwright, P. C. (2004). Motor pattern control for increasing crushing force in the striped burrfish ( Chilomycterus schoepfi ). Zoology 107 335346. LaBarbera, M. and Merz, R. A. (1992). Postmortem changes in strength of gastropod shells: evolutionary implications for hermit crabs, snails, and their mutual predators. Paleobiology 18 367-377. Lailvaux, S. P. and Irschick, D. J. (2007). The evolution of performance-based male fighting ability in Caribbean Anolis lizards. American Naturalist 170 573-586. Lessa, R. P. and Almeida, Z. (1998). Feeding habits of the bonnethead shark, Sphyrna tiburo from Northern Brazil. Cybium 22 383-394. Lindsay, G. J. H. (1984). Distribution and function of digestive tract chitinolytic enzymes in fish. Journal of Fish Biology 24 529-536. Lou, F., Curtin, N. A., and Woledge, R. C. (2002). Isometric and is ovelocity contractile performance of red muscle fibres from the dogfish Scyliorhinus canicula Journal of Experimental Biology 205 1585-1595. Martin, A. (1993). Hammerhead shark origins. Nature 364 494. Martin, A. P. and Palumbi, S. R. (1993). Protein evolution in different cellular environments: Cytochrome b in sharks and mammals. Molecular Biology and Evolution 10 873-891. Matott, M. P., Motta, P. J., and Hueter, R. E. (2005). Modulation in feeding kinematics and motor pattern of the nurse shark Ginglymostoma cirratum Environmental Biology of Fishes 74 163-174. Motta, P. J. and Wilga, C. D. (2001). Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environmental Biology of Fishes 60 131156. Papastamatiou, Y. P. and Lowe, C. G. (2005). Variations in gastric acid secretion during fasting between two species of shark. Comparative Biochemistry and Physiology Part A 141 210-214. Papastamatiou, Y. P., Purkis, S. J., and Holland, K. N. (2007). The response of gastric pH and motility to fasting and feeding in free swimming blacktip reef sharks, Carcharhinus melanopterus Journal of Experiment al Marine Biology and Ecology 345 129-140.

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152 Pinkas, L., Oliphant, M. ., and Iverson, I. L. K. (1971). Food habits of albacore, bluefin tuna, and bonito in California waters. California Department of Fish and Game, Fisheries Bulletin 152 Ramsay, J. B. and Wilga, C. D. (2007). Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks ( Chiloscyllium plagiosum ). Journal of Morphology 268 664-682. Sasko, D. E., Dean, M. N., Motta, P. J., and Hueter, R. E. (2006). Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus Zoology 109 171-181. Schenk, S.C. and Wainwright, P.C. (2001). Dimorphism and the functional basis of claw strength in six brachyuran crabs. Journal of Zoology London 255, 105-119. Summers, A. P. (2000). Stiffening the stingray skel eton an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). Journal of Morphology 243 113-126. Summers, A. P. and Long Jr., J. H. (2006). Skin and Bones, Sinew and Gristle: The mechanical behavior of fish skeletal tissues. In Fish Biomechanics vol. 23 Eds. R. E. Shadwick and G. V. Lauder pp. 141-177. San Diego, CA: Elsevier Academic Press. Summers, A. P., Ketcham, R. A., and Rowe, T. (2004). Structure and function of the horn shark ( Heterodontus francisci ) cranium through ontogeny: development of a hard prey specialist. Journal of Morphology 260 1-12. Toro, E., Herrel, A., and Irschick, D. (2004). The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. American Naturalist 163 844-856. Turingan, R. G., Wainwright, P. C., and Hensley, D. A. (1995). Interpopulation variation in prey use a nd feeding biomechanics in Caribbean triggerfishes. Oecologia 102 296-304. van der Meij, M. A. A. and Bout, R. G. (2000). Seed selection in the Java Sparrow ( Padda oryzivora ): preference and mechanical constraint. Canadian Journal of Zoology 78 1668-1673. van der Meij, M. A. A. and Bout, R. G. (2006). Seed husking time and maximal bite force in finches. Journal of Experimental Biology 209 3329-3335. Van Wassenbergh, S., Aerts, P., and Herrel, A. (2005). Scaling of suction feeding kinematics and dynamics in the African catfish Clarias gariepinus Journal of Experimental Biology 208 2103-2114.

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153 Verwaijen, D., Van Damme, R., and Herrel, A. (2002). Relationships between head size, bite force, prey handling efficiency and diet in two sympat ric lacertid lizards. Functional Ecology 16 842-850. Wainwright, P. C. (1988). Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69 365-645. Wainwright, S. A., Biggs, W. D., Currey, J. D., and Gosline, J. M. (1976). Mechanical Design in Organisms. Princeton, New Je rsey: Princeton University Press. Wainwright, P. C., Bellwood, D. R., West neat, M. W., Grubich, J. R., and Hoey, A. S. (2004). A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biological Journal of the Linnean Society 82 1-25. Westneat, M. W. (2003). A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223 269281. Westneat, M. W. (2004). Evolution of levers and linkages in the feeding mechanisms of fishes. Integrative and Comparative Biology 44 378-389. Wilga, C. D. and Motta, P. J. (2000). Durophagy in sharks : feeding mechanics of the hammerhead Sphyrna tiburo Journal of Experimental Biology 203 2781-2796.

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154 Figure 3.1. Feeding musculature of Sphyrna tiburo QMV = quadratomandibularis ventral, QMD = quadratomandibularis dorsa l, POV = preorbitalis ventral, POD = preorbitalis dorsal. Redrawn and modified from Wilga and Motta, 2000. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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155 Figure 3.2. Percent contribution of each feed ing muscle to bite force. Average standard error. Multiple linear regression showed that the only va riable that predicted theoretical bite for ce was QMD (p = 0.025). All other muscles had no predictive power due to their non-linear relationshi p to theoretical bite force. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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156 Figure 3.3. Typical crushing force curve for a 40.5 mm CL, 67.5 g C. sapidus crushed at a loading rate of ~370 mm/s using jaws removed from a 78.4 cm PCL S. tiburo Force increases to a maximum where failure occurs (black arrow). N = Newtons Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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157 Figure 3.4. Blue crab, C. sapidus crushing results from fr acture experiments on live crabs. Failure forces ranged from 30.0 to 490.0 N and exhibited a linear relationship to carapace length (CL) (y = 11.07x – 308, R2=0.87). Scaling anal yses indicated that failure force scaled isometrically with carap ace width and length. However, failure force scaled with positive allometry with car apace depth and mass. N = Newtons Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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158 Figure 3.5. Occurrence of blue crabs, C. sapidus in the stomachs of S. tiburo from Corts et al. (1996). Highlighted bo x (dashed blue vertical line s) indicates th e size range of sharks used in this study. Red solid line is the range of maximum size crab S. tiburo of 55.2-68.7 cm PCL is capable of crushing ( 32.3 – 37.5 mm CL, dashed red lines) based upon the maximum and minimum bite force. The majority of C. sapidus ingested by sharks can be crushed. However, crabs consumed that fall above the solid red line (~21%, green points) cannot theoretically be crushed by sharks of this size range and would require other processing methods. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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159 Figure 3.6. Anterior and posterior mechanical advantages for durophagous chondrichthyans studied to date. Dark line at mechanical advantage = 1 is the point where the lever system switches from a third class lever system to force amplifying a second class lever system. Sphyrna tiburo consumes hard prey w ithout the advantage of a second class lever system. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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160 Table 3.1. Average force and mass standard error of the four principal jaw adducting muscles in S. tiburo Muscle Force (N) Mass (g) Quadratomandibularis Ventral 33.2 2 1.37 0.1 Quadratomandibularis Dorsal 17.4 0.8* 0.96 0.1 Preorbitalis Ventral 27.7 1.4 2.43 0.1 Preorbitalis Dorsal 17.8 1 1.35 0.1 Data represent raw muscle values from 10 S. tiburo (x mass = 2440 g). Changes in the quadratomandibularis dorsal unresolved force was posi tively related to bite force (* p=0.025). No other muscle force or mass wa s related to output bite force. N=Newtons Reproduced with permission from Mara et al., 2010; Journal of Experimental Zoology.

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161 Table 3.2. Average maximum bite force (N) standard error for Sphyrna tiburo in each testing condition. Variable Restrained Stimulated Theoretical Anterior BF 14.2 1.2* 17.3 2.1 20.0 1.4* Posterior BF 53.1 5.2** 64.6 8.3 77.4 5** Max Anterior BF 20.3 25.3 25.7 Max Posterior BF 79.2 91.1 107.9 Theoretical bite force was grea ter than restrained bite for ce for anterior (* p=0.017) and posterior (** p=0.014). Maximum bite forces ar e the single largest force for any of the sharks. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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162 Table 3.3. Comparison of absolute bite fo rce and size-removed b ite force residuals among fishes. Species Common Name Mass (g) Anterior Bite Force (N) Residual Bite Force Chilomycterus schoepfi4 striped burrfish 180 380 1.92 Lachnolaimus maximus2 hogfish 209 290 1.65 Archosargus probatocephalus1 sheepshead 581 186 0.89 Heptranchias perlo8 sharpnose sevengill 1614 245 0.68 Carcharhinus limbatus6,8 blacktip shark 9833 423 0.35 Heterodontus francisci5,8 horn shark 2948 206 0.30 Hydrolagus colliei7 spotted ratfish 870 106 0.30 Halichoeres bivittatus2 slippery dick 19 11 0.19 Chiloscyllium plagiosum7 white-spotted bamboo shark 870 106 0.07 Halichoeres garnoti2 yellowhead wrasse 21 10 0.07 Thalassoma bifasciatum2 bluehead wrasse 7 5 0.00 Sphyrna mokarran9 great hammerhead 580598 2432 -0.04 Negaprion brevirostris7 lemon shark 1219 79 -0.06 Carcharhinus leucas9 bull shark 140341 1023 -0.11 Halichoeres maculipinna2 clown wrasse 18 5 -0.41 Squalus acanthias3 spiny dogfish 1065 19.6 -1.05 Sphyrna tiburo bonnethead shark 2240 25.7 -1.16 Etmopterus lucifer8 black belly lanternshark 48 3.1 -1.18 Etmopterus spinax8 velvet belly lanternshark 349.1 1.6 -2.47 Highlighted species have a predominat ely durophagous diet. Compiled from 1Hernndez and Motta, 1997; 2Clifton and Motta, 1998; 3Huber and Motta, 2004; 4Korff and Wainwright, 2004; 5Huber et al., 2005; 62006; 72008; 82009; 9Huber and Mara, unpublished data. Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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163 Table 3.4. Scaling of crab carapace properties with respect to length, width, depth, and mass. Dependent Variable Independent Variable Isometric Slope Slope yintercept r2 t ( 0.05 ( 2 ), 16 ) t critical Failure Force (N)Carapace Width 2 2.38 -2.28 0.871.63 2.12 Carapace Length 2 2.51 -1.95 0.862.03 2.12 Carapace Depth 2 2.63 -1.48 0.832.12 2.12 Crab Mass 0.67 0.87 0.71 0.852.22 2.12 Failure force scaled with positive allometry to carapace depth and crab mass (*, p 0.05). Reproduced with permission from Mara et al ., 2010; Journal of E xperimental Zoology.

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164 OVERALL CONCLUSIONS The overall goal of this study was to inve stigate the evolution and function of the hammerhead cephalofoil and the consequences of changes in head shape and form on the feeding morphology and sensory structures, an d any resulting constr uctional constraints within the cephalofoil. For the first part of this study, I investigated the changes in external morphology through phylogeny along with the potential constructional constraints within the cranium. The goals of th e first part of this were to 1) investigate the shape changes of the sphyrnid head through phylogeny; 2) examine the volumetric changes of cephalic elements through phyl ogeny; and 3) investigate potential constructional constraints between and among feeding, neural, and sensory structures. Through phylogeny the position of the eye a nd nares is variable; however, there are few changes to the relative position of the mouth. The position of the eye shifted laterally through phylogeny and to a more po sterior position on the distal tip of the cephalic wing. The external nares are medi ally placed in basal species and through phylogeny shifed first laterally and then medi ally again. Despite changes to cephalic morphology the electrosensory system is relati vely conserved within sphyrnid and closely related carcharhinid species with all species except ( C. acronotus S. mokarran and S. lewini ) having the same number of dorsal and ventral pores. Carcharhinus acronotus S. mokarran and S. lewini all had a significantly greater number of pores on the ventral surface of the cephalofoil. Despite E. blochii not differing markedly from other sphyrnid sharks in pore distribution, it lacks pores along the anterior su rface of the ventral

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165 cephalofoil. This is most likely related to the position of the nares and their affect on the anterior lateral pore field. In light of the external morphometric changes to the cephalofoil through phylogeny, ch anges to the internal cr anial volumes were also expected. This portion of the study also determined that, through evolutionary history, there are few constructional constraints among the various elements within the cranium. The few constraints were isolated to sens ory structures. Nasal capsule volume was negatively correlated with brain case, basihyal, chondrocranial, and total volumes. As the volumes of these cranial structures increases th e volume of the nasal capsule is decreased. The other constraint of note is the negative correlation betw een eye size and cephalofoil width. As width of the head increases its de pth decreases to keep the volume constant, consequently the volume of the eye is constrai ned to be smaller. Within the cephalofoil there were also elements that were pos itively correlated through phylogeny. Positive correlations were particularly apparent am ong the volumes of the feeding muscles and jaw cartilages. For these biting sharks, the volume of the jaws and supportive cartilages increase in size as the adductive muscle that ar e attached to them increase in size. These findings also indicate that although the head has changed in form through evolutionary history, there have been no major change s to the internal cranial volumes. These data indicate that much of the h ead is morphologically conserved through sphyrnid phylogeny, particularly the jaw cartila ges and their associated feeding muscles, with shape change and constructional constrai nts being primarily confined to the lateral wings of the cephalofoil and its associated se nsory structures. Ancestral character state reconstructions agree with previous analyses that the common ancestor to all hammerhead sharks was large bodie d with a relatively large head.

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166 The second portion of this study was focused on describing the functional morphology of the feeding apparatus of hamme rhead sharks. While feeding morphology has been described for a single species of hammerhead shark, S. tiburo a detailed study of the feeding apparatus thr ough phylogeny is requ ired to answer que stions about the effects of changes in head morphology on feed ing structures. The goals of the second part of this study were to : 1) describe and compare the functional morphology and biomechanics of the feeding apparatus of th e hammerhead sharks; 2) investigate if changes to the feeding bauplan exist in sphyrnid sharks or if changes are confined to surrounding structures with cons ervation of the feeding appara tus; and 3) investigate the relationship between cranial design and feeding morphology through phylogeny in this clade. Through phylogeny changes to the cephalofoil are mainly confined to the sensory structures and chondrocranium. Furthermore, the feeding ba uplan is conserved within sphyrnid sharks compared to closely related carcharhinid sharks with few changes to the feeding structures and feeding biomechanics. Sphyrnids as a group have relatively low anterior mechanical advantages that are similar to low to intermediate jaw leverage systems in teleosts. Within elasmobranch s the anterior mechanical advantage is somewhat lower than that of other piscivorous elasmobranchs. Anterior bite force is best predicted by the force produced by the preorbitalis ventral muscle while posterior bite force is best predicted by not only the force produced by the preorbitalis ventral but also the force produced by the preorb italis dorsal and the posterior mechanical advantage. Size-removed bite force analysis indicated that in general sphyrnid sh arks have lower bite forces for their body size than closely related carcharhinid sharks. Furthermore, the lone

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167 durophagous sphyrnid, S. tiburo had among the lowest aver age residual bite force. Surprisingly, this analysis also revealed th at the width of the cephalofoil had no effect on feeding morphology. However, positive correla tions were found between the anterior mechanical advantage and the volumes of the POV, palatoquadrate, Meckel’s cartilage, and hyomandibula. Paradoxically, this study also revealed th at posterior bite force was negatively correlated with the volume of the POV, POD, palatoquadrate, Meckel’s cartilage, and hyomandibula despite these structures’ role in force production and transmission. The reasons for these surprisi ng negative correlations remain elusive but may be related to changes in lever mechanics, particularly changes to the weighted inlever through phylogeny. Furthermore, although volume is an accurate measure of muscle size, it does not necessari ly reflect the cross sectional area of the muscle. Cross sectional area determines the force produced by the muscle, and it is the force produced by the POV and POD that were best predictiv e of posterior bite force not the volume. The final portion of this study investigated bite force and feeding performance in the durophagous hammerhead, S. tiburo Durophagy in Sphyrna tiburo is an ecomorphological conundrum as they cons ume hard prey but lack many of the characteristics associated with durophagy in other chondrichthyans. The goals of this third portion were to: 1) characterize the m echanical function of the feeding mechanism of S. tiburo through biomechanical modeling of b iting and bite force measurements obtained via tetanic stimulation of jaw muscles and restraint of live animals; 2) compare the bite force of S. tiburo with those of other fishes; and 3) identify functional constraints on prey capture and diet by co mparing the bite force of S. tiburo to the fracture properties of its primary prey item, blue crabs Callinectes sapidus

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168 The manner in which S. tiburo consumes hard prey is biomechanically different than has been described previo usly in chondrichthyans. It has relatively low bite force and lacks the hypertrophied jaw adducting musculature and jaws found in other durophagous taxa. Furthermore, when posterior mechanical advantage is compared among durophagous species, S. tiburo is considerably lower. Mass specific bite force analysis indicates that S. tiburo has among the lowest size-removed bite fo rces of any fish species measured to date. Wh en the bite performance of S. tiburo is compared to the mechanical properties of its known prey, it was discovered that S. tiburo consumes crabs that it is biomechanically in capable of crushing. Instea d, various methods of prey manipulation and processing are likely utilize d to consume large un-crushable crabs. Durophagy in the bonnethead indicates that durophagy can be accomplished without the morphological modifications seen in other durophagous taxa. While I described the morphometric changes to cephalofoil, the internal volumetric differences among species, the constructional constraints among internal elements, and the functional morphology of the feeding apparatus; there are clearly some areas that deserve further at tention. Of particular interest are the biomechanical consequences of the expanded cephalofoil on the structural and materi al properties of the chondrocranium in sphyrnid sh arks. Furthermore, the mo rphology and biomechanics of shark teeth have been shown to differ among shark species. Within sphyrnid sharks, tooth morphology ranges from large serrate d teeth to pavement-like teeth. An investigation of the functiona l morphology of sphyrnid teeth could elucidate differences in tooth morphology related to diet. I also did not sample every species of hammerhead (six out of eight). Although it is unlikel y that the overall patterns will change

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169 considerably, it is possible th at upon inclusion of the remaining sphyrnid species further constraints among internal elements will arise. Furthermore, while the sensory systems of this group of sharks have been investigated previously, more detailed work is needed on adult specimens, especially of the basal sp ecies, to truly understa nd the evolutionary pressures that resulted in the expanded cephalofoil. My study’s findings of few constructional constraints within the cephalofoil and lack of change to the feeding structures, along with the data of others, poi nts strongly toward sensory systems as the selective pressure resulting in the evolution of the cephalofoil. However, this research cannot rule out the po tential hydrodynamic role of the cephalofoil.

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ABOUT THE AUTHOR Kyle R. Mara was born in Kennett, MO on 11 – February, 1980 and spent much of his younger years on Minot Air Force Base, ND. Here he gained an appreciation for nature and began to nurture his inte rest in elasmobranchs. U pon graduating from Senath – Hornersville High School in 1999, Kyle went to Southeast Missouri State University and received his B.S. in Biology. Kyle then moved to Tampa, FL to begin his doctorate at the University of South Florida under the guidan ce of Dr. Philip J. Motta on the evolution and functional morphology of the hammerhead ce phalofoil. He has taught many courses from general biology to comparative vertebra te anatomy, and receiv ed a certificate of appreciation for outstanding graduate teaching assistant. Upon comp letion of his degree, Kyle has authored five papers.