You are on page 1of 173

University of South Florida

Scholar Commons
Graduate Theses and Dissertations Graduate School

1-1-2014

Functional Morphology and Feeding Mechanics of
Billfishes
María Laura Habegger
University of South Florida, mhabegge@mail.usf.edu

Follow this and additional works at: http://scholarcommons.usf.edu/etd
Part of the Integrative Biology Commons, and the Physiology Commons

Scholar Commons Citation
Habegger, María Laura, "Functional Morphology and Feeding Mechanics of Billfishes" (2014). Graduate Theses and Dissertations.
http://scholarcommons.usf.edu/etd/5617

This Dissertation is brought to you for free and open access by the Graduate School at Scholar Commons. It has been accepted for inclusion in
Graduate Theses and Dissertations by an authorized administrator of Scholar Commons. For more information, please contact
scholarcommons@usf.edu.

Functional Morphology and Feeding Mechanics of Billfishes

by

María Laura Habegger

A dissertation submitted in partial fulfillment
of the requirements for the degree of
Doctor of Philosophy
Department of Integrative Biology
with a concentration in Physiology and Morphology
College of Arts and Sciences
University of South Florida

Major-Professor: Philip J. Motta, Ph.D.
Stephen Deban, Ph.D.
Henry R. Mushinsky, Ph.D.
Daniel Huber, Ph.D.

Date of Approval:
November 10, 2014

Keywords: biomechanics, rostrum, anatomy, performance.

Copyright © 2014, María Laura Habegger

DEDICATION

To my family for their endless support, for teaching me to do my best and never give up.

To Martin for his patience, his support and his fuelling love.

To Phil and Diane for making us feel we were not alone, for giving us a family away from home.

advice. I never felt alone. I would like to thank each member of my committee. Thank you for believing in my work. a source of unbelievable knowledge and an invaluable friend. Yes!. for sharing his knowledge and amazing ideas and Henry Mushinsky for his understanding. they were always there for me. ACKNOWLEDGMENTS I would like first and foremost to thank my advisor Dr. for opening the door of his lab to me twice. for providing so many thorough suggestions. Gray . Mary. most of my family and friends but I know without hesitation that I would do it all over again with him as my advisor. for accommodating a five minute meeting without previous notice in his busiest day. Ryan and Karen at the office for solving every single logistical issue an international student may have. Dan Huber who has been an incredible support. John Dunlop. It wasn’t easy being away from home. I would not have done a fraction of what I accomplished today without his continuous support. Marc Lajeunesse. for your encouragement. Steve Deban for always have time for me. David Johnson. for you endless support and time. I spent enough time here to have them all…. Thank you to Christine. Thank you so much! I could not have done this research without the collaboration of many remarkable scientists that I deeply admire. I deeply admire you all as scientist but foremost I’m incredible happy I got to know you through these years to learn how amazing people you all are. However. Philip Motta for being an incredible mentor. I still cannot believe I got to work with all of them! Endless thanks to Mason Dean. You are a second father to me. Betsy Dumont. his support.

For sharing years of his work with me. for believing in me. for leaving everything else to be here. Thank you to Candy Miranda and Ed Haller for his patience teaching me how to use the SEM. Harry Fierstine one of the most important researchers in the billfish arena. To Angela for her support. To my family. for your generosity and support. your patience. Endless thank you to Martin. Thank you to Jose for being there since the beginning. Thank you to Summer Decker and Jon Ford for opening their lab to me for making me a little bit better with computers. . for making my collecting summers so amazing. I’m deeply grateful to Dr. Bob Hueter. for his time and generosity. Thanks to Aliza Karim. for teaching me and for their support. To Pilar for her encouragement. Jayne Gardiner. thank you for living this with me. it is such an honor! Special thanks go for Anna Avrigian and Jim Franks. You are the most generous person I know. I could not have made it this far without you. Jack Morris and Mote marine laboratory. thank you to Anne Barse. your encouragement and understanding. without you I would not have this project done. thank you for teaching me my work ethics and for guiding me and encouraging me to do my best even if it was the difficult way.Mullins and Michael Stokes. my partner in many fish adventures that occupy a special place in my heart. Many thanks to my good friend Sam. your love fuels my life and this accomplishment is also yours. Amber Ferguson. Christopher Heffner and Vera Melnichuk. your support had fuelled me through the years. Doug Perrine and Captain Ed Walker for allowing me to use your beautiful artwork. Thank you Rafael de la Parra. for his encouragement. Richard Stanczyk. hugs and sweet words. for his welcoming support and encouragement. Other people have been immensely generous towards my research by providing specimens. for showing me that pure friendship can be acquired later in life. Thank you teaching me to be better every day and not give up.

.......13 Histology ...10 Material and methods ......................................35 Chapter Three: Feeding biomechanics in billfishes: investigating the role of the rostrum through finite element analysis .26 Biological loading scenarios: Point loading and hydrodynamic loading...............................................................................................65 Discussion ....................................................66 i ....................................................................................................24 Bending experiments in a material testing system (MTS) .................................................................................................................................................................................................................................................................................................................................................................................................................................56 Introduction ........................................................................................................................................................9 Introduction .....................................................................................................................................................................28 Discussion .......................56 Abstract ..6 Chapter Two: Feeding in billfishes: inferring the role of the rostrum from a biomechanical standpoint.57 Material and methods ............................... iv List of Figures .................................................................24 Geometric analysis ........................................................................................................................................................................................................................................................64 FEA models ................................................................................................................................................................18 Biological loading scenarios: Point loading and hydrodynamic loading.........................14 Geometric analysis .................................................................................................................................................14 Bending experiments in a material testing system (MTS) .........................................................................64 Model validation ...........................................................................63 Results ........................................................................................ viii Chapter One: General Introduction ..........................................................................................................................................................v Abstract ..................................................................................................... TABLE OF CONTENTS List of Tables ......................................................................................28 References ................................................................................................................................................................................................................................................................1 References .........................................................................................................................9 Abstract .........................24 Histology ..........................................................60 Model Validation ....................................................................................................................................................................20 Results ...........................................

...................................99 Rostrum evolution......................................................134 Chapter Six: Final Conclusions ........................................................................................................................................124 Warping: qualitative analysis of the major trends in the skull of billfishes...................................................................................................................................... References ..............................................................................................................................88 Theoretical calculations of bite force .....................................................................156 ii ................................................................................126 Correlation assessment in raw and phylogenetically corrected variables ..........................................................................90 Bite force within billfishes ......................97 Bite force comparison .............127 Possible trade-offs ................................................................................................116 Abstract ..........................................................................................................................85 Material and methods .............................................................................................129 Overall changes in morphology and feeding performance implications ..............................................................................................................................................126 Discussion ..........................................................................................................................101 References ..............................................................88 Anatomical descriptions.95 Bite force within billfishes ..........................................96 Bite force among billfishes ..............93 Bite force and biomechanical parameters ...........................................................................................................................................................................................................................................................................................................................153 Appendices ....................................................................................................94 Bite force predictors .................................................................................................121 Landmarks description ...........103 Chapter Five: Geometric morphometrics of the billfish skull .........................................................92 Bite force among billfishes ........................................................................96 Discussion ......................................................................................................................................................................................................................................................73 Chapter Four: Feeding biomechanics and theoretical calculations of bite force in billfishes ...............89 Bite force predictors ....127 Changes between billfish rostra and the skull................................................................................................................................................................................................................................121 Landmarks analysis ..................84 Abstract ............................................................................................................84 Introduction .................125 Principal components analysis ..............................................................................................................................122 Results .................................................................................................................................116 Introduction ...................................................................96 Bite force in billfishes .......................................................................................................................................................................96 Bite force predictors .......130 References ..........124 Changes within istiophorids........................................................................................................................................................................................................................................................................................................................................................93 Results ........................................147 References .................................................................117 Material and methods ..................................................................................93 Anatomy............................................................................................

........................................157 Appendix B: Permission to utilize MATLAB scrip and photographs for this research ......158 iii ...................................................Appendix A: IACUC Protocol approval....................................................................................... ...............

......4: Mass specific bite force in billfishes vs “non billfishes”...................................110 Table 5.................................109 Table 4........ loadings and variance for five billfish species and wahoo (A...............3: Specimen information .................................................. LIST OF TABLES Table 2..............................................108 Table 4................................................................1: List of 55 landmarks utilized in 3D analysis in five species of billfish and the wahoo (A.......................1: Raw mean values ± SD of bite force and biomechanical variables for billfishes and wahoo (A.......... solandri) ..............................................2: Experimental and predicted stress means (MPa) compared for FE model validation...............140 Table 5....................... nigricans) during three loading regimes .......78 Table 4.................................................. swordfish (X.2: Standardized values of stress obtained from bending experiments in blue marlin (M...................... nigricans) ...............107 Table 4..............1: Second moment of area obtained from MATLAB geometrical analysis along the rostrum of two billfish species............. gladius) and blue marlin (M........................... gladius) and blue marlin (M.141 iv .......43 Table 2........................42 Table 2............................................................................................. solandri) .......................3: Mass specific bite force (mean ± SD) within billfishes ........................77 Table 3.....................................................................................2: Results from PCA............................................................................44 Table 3...........................2: Model selection of bite force predictors based on AICc values among billfishes and wahoo (A.1: Stress values (A) and total strain energy (B) in two billfish species the swordfish (X..................................................................................................... nigricans) .. solandri) ................... solandri) ........................................

. 100 % = proximal base) of swordfish (X.............. hydrodynamic load scenarios in a swordfish (X....... gladius) .. 2...............52 Fig.............8: Interspecific comparisons of standardized stress (N/mm2) from bending experiment in two loading planes ........ 2..................... 2........................................ 2...................................................48 Fig.... nigricans) on the right) ..................................... ............................................. ........... nigricans) ..10: CT scan reconstruction of a swordfish (X. n=4) and blue marlin (M......... mean ± SE..................49 Fig............. albicans) feeding event in Isla Mujeres.. . 2........................ gladius) rostrum................................ gladius) (right column..............54 Fig.......... gladius) with dorsal and lateral views of suggested loading regimes..6: Results from geometrical analysis along the length of the rostrum (0 % = distal tip.................... 2..................... 2.......................... 2........................47 Fig............................. Mexico .. gladius) values on the left and blue marlin (M..55 v ..................50 Fig...... swordfish (X................... 2..............46 Fig.....4: Results from histological analysis performed along four regions of the rostrum of a swordfish (X...............................................................................................7: Intraspecific results from bending experiments in two loading planes (mean ± SE.11: Injuries in prey items after a sailfish (I...................... gladius) rostrum .................................3: Simulated point load vs..........1: Illustration of the cross-sectional shape differences between species and description of the major steps performed during the MATLAB geometric analysis ................................................. nigricans) (left column........................ mean ± SE.................. LIST OF FIGURES Fig................................. n=2)....................51 Fig............2: Outline of the apparatus settings for the bending experiments on the material testing system (MTS) during lateral loading on a swordfish (X.....................................................53 Fig.........................5: Results from histological analysis performed along four regions of the rostrum of a blue marlin (M.........................................45 Fig............................. 2....9: Comparisons of localized and continuous loads among species and loading orientations ............ 2.....

.................144 Fig... shorbill spearfish T....... nigricans.. 4......3: Outline of the adductor mandibulae complex (deeper subdivision A3) in three representative billfishes (complete rostrum not shown) and wahoo (A. nigricans.............................81 Fig..115 Fig..... 4...... 3...... gladius..3: Lateral and dorsoventral view of the skulls of the six fish species investigated ............... gladius) rostrum during lateral loading showing the areas of stress used to validate FEA model’s geometries ....... and a non-billfish outgroup species (wahoo: A.....................3: Predicted von Mises stress distribution in the blue marlin rostrum (M...............80 Fig.......2: Predicted von Mises stress distribution in the swordfish rostrum (X..... 5.......... 5........................... shortbill spearfish: T............145 vi ...112 Fig............................................. 4................................ 5.....114 Fig.................. albidus and a non-billfish species used as the outgroup (wahoo................. audax).....143 Fig.... angustrirostris. 3............................................ a closely related species to blue marlin with similar rostrum morphology........................................... nigricans) for three loading regimes A) dorso-ventral.................................... albicans.....83 Fig............... 3..........4: Stress distribution (mean±SE) along 55 points of the rostrum in swordfish (X.................. gladius) for three loading regimes A) dorso-ventral........ 3.... solandri) ...82 Fig............ solandri) .. gladius...113 Fig.................. A solandri) . albicans and white marlin T........................................... B) lateral and C) axial loading...........................5: Spearing event in a striped marlin (K....... sailfish: I.2: Phylogenetic relationships among five billfishes species (blue marlin: M. solandri) ........ gladius) (left) and blue marlin (M....2: Outline of the adductor mandibulae complex (superficial subdivision A1+A2) in three representative billfishes (complete rostrum not shown) and wahoo (A.............................. .... angustrirostris.. indica) representing all landmarks utilized in six species of fishes............... . swordfish X..Fig..... swordfish: X..... 4....................1: Left lateral and dorso-ventral view of blue marlin (M.. sailfish I........ B) lateral and C) axial loading .......... solandri) ...........................4: Principal component analysis of 55 3-Dimensional landmarks in five species of billfish and the wahoo (A...................................................142 Fig... white marlin: T. ...1: Outline of the experimental settings and the FEA results of a swordfish (X.........3: Relative bite force within billfish and outgroup wahoo (A solandri) ................................................. albidus..........................1: Phylogenetic relationships among five billfishes species (blue marlin M. 3. 5........................................79 Fig... nigricans) (right) during lateral loading (black dots) and dorso-ventral loading (white dots)..

.5: Regression and correlation matrix of 17 linear variables obtained from five billfish species and the wahoo (A.......... 5.......... solandri) ...........Fig.....................146 vii .............

either stunning or cutting them into pieces before ingestion. By the use of interdisciplinary approaches that blend engineering with biology. Billfishes have been observed to subdue their prey with their rostrum. Results showed that the rostrum in billfishes is mechanically capable of acting as a feeding weapon. By the use of different approaches that involve morphological characterizations. histology. and perhaps their most recognizable attribute is their bill or rostrum. spearfishes. However. the most supported hypothesis for its function has been linked to feeding. continuous stress distribution along its length suggest no particular point that could lead to breakage during feeding. The proposed function for this novel structure has ranged from hydrodynamic enhancement to defensive weaponry. my dissertation aims to characterized the role of the rostrum in billfishes as a possible adaptation for feeding. as well as bending experiments suggest feeding behavior may be species specific and strictly associated with rostrum morphology. estimation of performance measurements such as bite force and the investigation architectural tradeoffs from geometric morphometrics analysis. While viii . mechanical and morphological standpoint. sailfishes and swordfish) are one of the fastest and largest marine apex predators. Due to their large body sizes and pelagic lifestyles a thorough investigation of the function of this structure has been logistically challenging. Finite element analysis. the function of the rostrum and billfish putative feeding behavior was investigated. ABSTRACT Billfishes (marlins. The goal of my dissertation is to investigate the role of the rostrum during feeding from a functional.

morphology and head architecture. Skull variation was evident among billfish species. The shortbill spearfish showed a relatively low bite force indicating predatory success in this species may be linked to an extended lower jaw that may facilitate a speed efficient jaw during prey capture. swordfish appear to be specialized from a mechanical and hydrodynamic standpoint to hit their prey with lateral strikes. remains uncertain. in addition to relatively low biting performance in billfishes. had the smallest head and the lowest relative bite force whereas blue marlin. ix . the species with the stiffer. Swordfish. most compact rostrum. the species with the longest rostrum. had the largest head and one of the greatest relative bite forces. Biting performance is relatively low in these top predators compared to other non-billfish species suggesting the rostrum may facilitate prey processing reducing the need for powerful biting. Whether the rostrum in billfishes has evolved as an adaptation for feeding. However contrary to my expectations rostrum length was not a predictor of bite force.istiophorids may be morphologically suited to strike their prey with a wide range of motions. However results from this study demonstrate that rostrum material properties. favor a role of prey capture for the rostrum.

From genotype to phenotype. this structure appeared to play a crucial role in vertebrate radiation (Cole and Friedman. Perhaps one of the most diverse structures is the skull of vertebrates. where multiple feeding guilds from piscivory to wood eating coupled with extreme morphologies can be found (Westneat. the largest vertebrate group. CHAPTER ONE GENERAL INTRODUCTION Organismal diversity is astonishing..e. 1990). Smith. Adriaens and Herrel. 2006. 2005). Novel structures may isolate functions diluting the need for structures to perform multiple tasks. 2012). 2009). or morphological standpoint. and from a physiological. and this novel structure allows for a functional decoupling from the oral apparatus resulting in an immense trophic diversification (Wainwright et al. the pharyngeal jaws in labrid fishes act as an independent set of jaws. 2005. This diversity is ignited within fishes. feeding. Novel structures can amplify this diversification. for 1 . 2012). breathing. housing major sensory organs). behavioral. Due to its complex integrated nature involving several important roles linked to survival (i. Feeding has been one of the major drivers of skull diversification as noted in the large structural and functional variation of their trophic apparatus (Schwenk. as evolutionary novelties provide the raw material for natural selection to act on (Jablonski. 2000. Hall. However novel structures may come with an associated cost. For example. organismal variation can achieve endless forms.

Organismal performance is the most important link between organismal phenotype and its ecological success (Santana and Dumont. Husak et al. 2012). 2009). Functional morphology is the field that explores diversity from a functional standpoint. 1983). providing an understanding of the selection on certain phenotypes and their functions. Biomechanical approaches have opened a window 2 . has been identified in different systems. The relationship between form. this approach has helped to identify the physical principles that explain how form differentiation can result in similarities or differences in their mechanical function (Koehl. in collared lizards (Crotaphytidae) performance measures including bite force and sprint speed were linked to head and limb architecture. The attainable nature of performance and its significance as a proxy for fitness has opened a window for many investigations where performance parameters such as bite force or sprint speed have been estimated (Irschick et al. 2006. 1996). 2006). 2008). Morphology may be perhaps the most perceivable approach for the quantification of organismal diversity. although not straightforward. Understanding organismal form not only helps us to characterize diversity but also improves our understanding of the ecological mechanisms that underlie it (Collar and Wainwright. Form can be related to function and fitness through performance (Arnold. Biomechanics is an interdisciplinary approach that encompasses the use of engineering in biological systems..example in beetles large strong jaws pose a tradeoff between handling ability and the utilization. 2006). For example. opening of new food niches (Konuma and Chiba. Not surprisingly the study of form is one of the most important contributors to its quantification (Hulsey and Wainwright.. Often used in functional morphology. function and fitness. 2002). and adults with high biting and sprinting performance showed higher reproductive success (Husak.

for the investigation of logistically challenging systems such as large predators or even extinct

ones.

Billfishes (marlins, spearfishes, sailfishes and swordfish) are one of the fastest and largest

marine apex predators but perhaps their most recognizable attribute is the extreme elongation of

their bill or rostrum (Nakamura, 1985, Davie, 1990, Fierstine, 1990, Fierstine and Voigt, 1996).

This novel structure that gives name to this group has been focus of many studies, however its

role remained speculative for decades (Nakamura, 1983, Frazier et al., 1994).

The billfish rostrum has been suggested to have an important role in hydrodynamics,

more specifically as a drag reducing device (Wisner, 1958, Ovchinnikov, 1970; Aleyev, 1977;

but see Sagong, et al. 2014). Another possible role is defense, evidenced from the encounters of

pieces of rostrum embedded in large predators such as sharks or other billfishes (Fierstine, 1997;

Fierstine et al., 1997). Finally, the rostrum was suggested to be used as a feeding weapon to

strike, immobilize or dismember prey before ingestion, thereby facilitating feeding (Gudger,

1940, Talbot and Penrith, 1964, Scott and Tibbo, 1968). The latter hypothesis was recently

supported in a field study where sailfishes (Istiophorus albicans) where filmed striking prey that

was later ingested (Domenici et al., 2014).

The billfish rostrum varies in size and shape among the 13 recognized billfish species,

however the greatest rostral disparity occurs between the families Xiphiidae and Istiophoridae.

The rostrum in swordfish (Xiphias gladius, Xiphiidae) is long, reaching length up to 50% of their

body, dorsoventrally depressed and edentulous. In general the rostrum in istiophorids is stouter,

no longer than 25 % of their body length and in some cases, such as in the shortbill spearfish

(Tetrapturus angustrirostris), only a few centimeters of length. Species specific feeding

behaviors have been suggested in billfishes with different rostrum morphologies, where

3

swordfish are suggested to slash their prey with only lateral movements of the rostrum (Scott and

Tibbo, 1968, McGowan, 1988), and istiophorids are described as stunning and/or spearing their

prey, thereby using a wider range of rostral movements (Talbot and Penrith, 1964; Fierstine,

1997; Fierstine et al., 1997; Shimose et al., 2007). However due to the logistical challenges

associated with the study of large and fast predators in the field this question still needs

clarification.

The goal of my dissertation is to investigate the role of the rostrum in billfishes from a

mechanical, functional and morphological standpoint. The logistical constraints of studying free

swimming and feeding billfishes offer a great opportunity for the use of functional morphology

and biomechanics to investigate the role of this novel structure as a possible adaptation for

feeding. Therefore the first part of this research, chapters two and three, focused on the

relationship among form-function and feeding ecology, paying special attention to the role of the

rostrum from a mechanical standpoint. By selecting the two most distinct rostra morphologies, I

aimed to characterize the material properties and the mechanical attributes of the rostra to

ultimate infer its role during feeding. This approach was performed by the use of beam theory

and strain gauges, and a custom designed script that characterized rostrum mechanical attributes

and histology. In this chapter I expected that if the rostrum is used for striking prey, large

deflections could be detrimental, consequently stress along the rostrum should be equally

distributed, hampering higher stress in any specific region that could lead to breakage. I expected

to see similar patterns in other variables such as flexural stiffness. Finally, based on interspecific

differences in rostrum biomechanics and morphology inferences about their species specific

feeding behaviors are proposed.

4

The third chapter covered similar questions proposed in Chapter 2, however the

utilization of an innovative approach used in engineering, finite element analysis, provided a

complementary analysis to the logistical limitations associated with the use of strain gauges and

beam theory. In this chapter I expected each rostrum morphology to be suited to better withstand

the loads associated with their most common feeding behaviors, for example in swordfish I

expected stress to be low when the rostrum was loaded in lateral direction compared to loadings

in dorsoventral direction. Chapter four deals with performance, specifically I investigated biting

performance in five billfishes. Since the rostrum may act as feeding weapon decoupling food

processing from the oral apparatus, I expected billfishes to have relatively low values of bite

force compared to other non-billfish species, since they can rely on their rostrum to preprocess

their prey. I also expected to see performance differences among billfish with different rostrum

morphology, where species with long rostrum such as the swordfish (Xiphias gladius), may have

lower bite force and species with shorter rostrum such as the shortbill spearfish (Tetrapturus

angustirostris) may have lager bite forces.

In the last chapter I investigated morphological variation and differences among the skull

of billfishes and the possible implications of shape changes in the skull to rostrum morphology in

an evolutionary context. Combined with previously obtained variables such as bite force, this

chapter investigated architectural trade-offs between within the skull and between the rostrum

and the skull. As observed in clariid fishes, head changes such as the reduction of skeletal

elements can be linked to feeding performance and the increase of adductor muscles and

consequently bite force (Devaere et al., 2001).

5

Fierstine. (2001). D. Copeia 1996. and Prigioni.. Adriaens. 347-361. The Hague. 1873) (Teleostei: Siluriformes): are adaptations related to powerful biting? J. Zool. 1988. J. (2009) Functional consequences of extreme morphologies in the craniate trophic system.G. R. (2006). Aleyev. Zool. H. A paleontological review of three billfish families (Istiophoridae. Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes.L. Cole Sallan. S.C. Soc. R. 1-6.L.L. 2575-2584. (1994). L. Palmerston North. doi: 10. Heads or tails: staged diversification in vertebrate evolutionary radiations. S. performance and fitness. Proc.. and Wainwright. G.2011. (1990). Fierstine.. P. Impalement of marine turtles (Reptilia. and Voigt.L. Y. Planning the future of billfishes.. Pitman. 82.G. and Friedman. P.2454. Evolution 60. (1983). Press. Devaere.. Frazier. Xiphiidae and Xiphiorhynchidae).References Adriaens. Kailua-Kona.J. Contributed papers. F.C. Pages 11-19 In R. Use of rostral characters for identifying adult billfishes (Teleostei: Perciformes: Istiophoridae and Xiphiidae).G. H. W. S. 148-161. Part 2.. Davie.M. Physiol. D. Junk. 23. Proc. Collar. Amer. A. Y. H. Arnold. Fierstine. B. Verraes. D. Morphology. (1990). 235-250. Hiroyuki. Yamaguchi. and Herrel. C. S.L. Hawaii. Nekton. 255. New Zealand Massey Univ. Achaval.. M. August 1-5. Beavers. Zool. Pacific Marlins: Anatomy and Physiology. H. ed.1098/rspb. (2012). and Teugels. N.C. Biochem. Stroud. Cranial morphology of the anguilliform clariid Channallabes apus (Günther. (1996). 2nd Int. Chelonia: Cheloniidae 6 . Billfish Symposium. (1977).

Lab. 5. and Wainwright. 28.. Mem.H. Ecol. Ecol. 301- 306. Mapping mechanics into morphospace: disparity in the jaws of labrid fishes. Asiatic. Bite. 170. 10. Nat. Soc. FAO Species Catalogue. J.F. Husak. B. (2008). Biol. I.. 39.. M.. Res. (1996). Gudger. In: M. 215-31. J.. No.F.125. 501-542. I. University of Chicago Press. 2. Syst. J. Nakamura. J. vol. The ecology of evolutionary innovations: The fossil record. Evolutionary Innovations. D. 269. 90-100. Konuma. C. D. How does selection operate on whole-organism functional performance capacities? A review and synthesis. 27. (2007). Lemos-Espinal. FAO Fish. E.J.. Le Galliard. (1983). 7 . Env.A. Bengal Branch. S. Nitecki. Amer. (1940)... Lappin. Nakamura.W.F.J. ed. Jablonski. When does morphology matter? Ann. J. Synop. Husak. 253- 288. 85-96.J. Koehl. 177-196. K. Trade-offs between force and fit: extreme morphologies associated with feeding behavior in carabid beetles. J.F. (2006). Billfishes Of The World. D.A. Roy.317-326. and Dermochelyidae) by billfishes (Osteichthyes. Biol. (1985). Proceedings of the Royal Society. Rev.D. (2002). Seto Mar. London. and Bottjer.force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus). 1-65. The allegated pugnacity of the swordfish and the spearfishes as shown by their attacks on vessels.C. (1990). Evol. Perciformes: Istiophoridae and Xiphiidae). Irschick. Fox. Copeia 2006(7). Fish. Publ. S. and Chiba. Systematics of the billfishes (Xiphiidae and Istiophoridae).R. P. Meyers. Hulsey. 255-396..

1964.. Spearing behavior in feeding in the black marlin. Ferry. P. Ecology and Functional Morphology. Sci. (2012). Prog. 60-70. J. Sci. Evol.V.. W. Wainwright.C. and Dumont. (2009). The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Swordfish and billfishes in the Atlantic Ocean. Connecting behaviour and performance: the evolution of biting behavior and bite performance in bats.E. and Penrih. V.L. Santanta. Istioampax marlina.A.S.J. and Near.H. Sparks. Biol. (1970). 12. R. Biol. 61. 2131-2145. T. K. Copeia.. NOAA NMFS TT 71-50011.J. F. Trans. Is the spear of istiophorid fishes used in feeding? Pac. 8 . Smith. S. Isr. Wisner. J. Talbot.Ovchinnikov. (1958)...A. S. (1964). 22. Syst. 1001-1027. E.L. 468. Tang. Price. J. L.R.

Histological samples and material properties of the rostra were obtained along their lengths to further characterize structure and mechanical performance. the blue marlin (Makaira nigricans) and the swordfish (Xiphias gladius). and morphological standpoint to ultimately infer its possible role during feeding. Surprisingly. CHAPTER TWO FEEDING IN BILLFISHES: INFERING THE ROLE OF THE ROSTRUM FROM A BIOMECHANICAL STANDPOINT Abstract Perhaps the most striking feature of billfishes is the extreme elongation of the premaxillary bones forming their rostra. Using beam theory. Intraspecific results show similar stress distributions for most regions of the rostra. The goal of this study is to investigate the use of the rostrum from a functional. the exact role of this structure in feeding is still controversial. Although material stiffness increased distally. experimental and theoretical loading tests were performed on the rostra from two morphologically different billfish. flexural stiffness increased proximally owing to higher second moment of area. Two loading regimes were applied (dorso-ventral and lateral) to simulate possible striking behaviors. suggesting this structure may be designed to withstand continuous loadings with no particular region of stress concentration. biomechanical. The blue marlin rostrum was stiffer and resisted considerably higher loads for both loading planes as compared to that of the swordfish. 9 .

Fierstine. The rostrum of swordfish (the only species within the Xiphiidae). 1970. spearfishes. Fierstine. The rostrum has been hypothesized to improve hydrodynamics by reducing drag (Wisner. simulating the rostrum swinging through the water. 1968). 1994. Scott and Tibbo. Although it is certainly possible that the elongated rostrum may have been selected for multiple roles.. Introduction The billfishes (marlins.. 1983. 1940. when a continuous load along the rostrum was considered. Domenici et al. thereby facilitating feeding (Gudger. suggesting the use of the rostrum in feeding is perhaps species- specific. substantial evidence from stomach contents. 2007. 1996). Fierstine and Voigt. 1997. and recent field observations strongly support the latter feeding-related hypothesis (Scott and Tibbo.However. Davie. immobilize or dismember prey before ingestion. 1964. The combined results of this study suggest the swordfish rostrum is suited for lateral swiping to incapacitate their prey. et al. Ovchinnikov. 1968. Fierstine et. Shimose et al. but see Sagong. 1985. 1958. 1990. Frazier et al. whereas the blue marlin rostrum is better suited to strike prey from a wider variety of directions. and to be used to strike. Talbot and Penrith.. 1997). al. 1994). Aleyev.. sailfishes and swordfish) are large and fast pelagic predators characterized by the extreme elongation of their upper jaw bones to form an elongated rostrum. 1990. 2014). The geometries and relative sizes of the rostra of different billfish species are in some cases strikingly different. swordfish exhibited lower stress and drag during lateral loading. or bill (Nakamura. to be used for defense (as evidenced by rostral fragments found embedded in large predators. 1985. which can exceed 10 .. Stillwell and Kohler. Surprisingly the function of this structure is still controversial (Nakamura. 1977. 2014). Frazier et al.

fast. Fierstine and Voigt. Gudger. and lacking teeth (Gregory and Conrad. distally tapered.. 1968. These structural differences between swordfish and marlin are indeed reflected in anecdotal accounts of feeding events. Habegger et al. enabling the quantification of mechanical performance and facilitating the inference of behavior from morphology. bull sharks and rorqual whales (Wroe et al. 1996. 1983. 2007). 2014). having sharp edges.. 1997. spearfishes and sailfishes). the rostrum is more circular in cross-section. 1940.. Correlations of these differences in rostral form and behavior between species.. Fierstine et al. 1937. 2003). Biomechanical approaches offer feasible ways to investigate the potentially differing roles of the rostrum in the various billfish species. being approximately 24% of body length in blue marlin (Gudger. Nohara et al. Fierstine. 2011. been nearly impossible to study due to the logistical issues associated with the study of large. Fierstine. Shimose et al. pelagic predators such as billfishes (but see Domenici et al. has no sharp edges.. 1997. thereby using a wider range of rostral movements (Talbot and Penrith. 1988). via investigations of feeding mechanics in white sharks. Nakamura. 1964. is wide..50% of body length. 2012). in istiophorids (marlins. and their mechanical implications at the tissue level have. The length of the rostrum varies among species but is proportionally shorter than in swordfishes. 1976. 1940.. and istiophorids are described as stunning and/or spearing their prey. 2008. 1983). The utility of these approaches has been demonstrated already for experimentally intractable taxa. Field et al.. McGowan. an engineering approach that describes the 11 . 1990. and dorsoventrally flattened with a lenticular cross-section. Poplin et al. Conversely. however. where swordfish are suggested to slash their prey with only lateral movements of the rostrum (Scott and Tibbo. and is surrounded by small villiform teeth. Nakamura. Significant advances in biomechanical studies have been accomplished through the utilization of beam theory.

Macleod. 2011. echinoderms. Baumiller. Etnier. A beam’s resistance to bending is given by the flexural stiffness. 1976. all of which can offer clues to loading regimes likely experienced in vivo. 2013). EI. σ. 1992). The goal of this study is to use biomechanical models and material testing to infer the possible biological role(s) of the rostrum in two billfish species with differing rostrum 12 .g. I or both. vertebral columns) (Koehl. 1993.. This approach is applicable because many biological structures can be treated as beams (e. from the limb skeletons of batoids and dogs. 1977. with stress distributions and yield behavior pointing to performance boundaries.mechanical behavior of a beam under loading. Huber et al. Ennos.. Macesic and Summers. trees. 1976.g. 2003). that builds in a material under load in response to deformation. to the exoskeletons of crabs (Kemp et al. Analyses of a structure’s cross-sectional geometry and the response of its material to load (e. I) (Koehl. Field et al.. which is a function of both its material properties (via Young’s modulus. these taxonomic comparisons also illustrate that higher levels of bending resistance can be attained evolutionarily by either increases in E. E) and its geometry (via second moment of area. Taylor et al. 2007. particularly when linking organismal function with evolutionary and ecological pressures (Koehl. 1980. Wainwright et al.. 1977. or stress. 2012). it is a useful metric for characterizing mechanical function in comparative studies. 1977. the force per unit area. or strain. to the jaws of whales and pelicans. Flexural stiffness has been shown to correlate with loading regime and direction for a range of biological body support systems. 2005. As EI accounts for both material and structural properties. ɛ) can therefore provide an understanding of the overall structure’s mechanical capabilities and limits. 1976. Biewener.. and beam theory also facilitates better comprehension of form and function relationships by allowing the teasing apart of factors that contribute to a biological beam’s performance under loading. 1993.

Tustin. Linnaeus. Inferences of the putative feeding behaviors of these two apex predators are then made based on these analyses.75-1. Heads were transported to the University of South Florida and frozen with the rostrum wrapped in plastic to reduce dehydration. samples were wrapped in plastic bags and kept frozen until material 13 . paying special attention to suggestions of how mechanical and growth demands may be balanced for these biological cantilevers.0 mm (image size 512x512 pixels.3) with intact rostra were obtained from fishing tournaments in the Gulf of Mexico. USA. I estimate several biomechanical variables and describe the material properties and geometric attributes of the rostrum along its length in order to acquire a better understanding of its function and mechanical capabilities.625 mm). Based on previous descriptions of cross-sectional geometry. 1758). Since failure or large deflections could be detrimental during feeding I hypothesize that stress will be equally distributed along the length of the rostrum. After being thawed all heads were CT scanned with a 64 slice Aquilon Toshiba scanner Toshiba American Medical Systems Inc. USA with slice thickness ranging from 0. 1802) and the swordfish (Xiphias gladius. Material and methods Four swordfish (Xiphias gladius) and two blue marlin heads (Makaira nigricans) (Table 2.morphologies. whereas that of the blue marlin will be suited for a larger range of motions. Utilizing beam theory as the primary model. Correspondingly. preventing any localized region of higher stress (“weak spots”) that could lead to failure during feeding. Lacepede. CA. pixel size 0. the blue marlin (Makaira nigricans. I expect that the swordfish rostrum will be better suited for lateral striking of prey. After scans were completed.. I expect flexural stiffness to be uniform along the length of the rostrum and sufficiently large to avoid appreciable deflections while striking prey.

Belgium). nuclei and osteocytes. these changes are irrelevant for the scale of my observations and osteocytes are lacking from the bone of these species. IACUC protocol number T 3884. Four transverse sections (areas 1-4. Pictures were taken at two magnifications.testing. mirroring the locations of strain gauge placement (see bending experiment section). distal to proximal) of approximately one half-centimeter thickness were cut from one representative rostrum of each species.. Transverse sections were preserved in 10 % buffered formalin followed by decalcification in formic acid (50 % HCOOH. transverse sections were prepared for both swordfish (n=1) and blue marlin (n=1) at four regions along each rostrum. Sections of 4 µm were made with a Bioacut microtome (Leica/Reichert Jung model 2030. 2008). Although this tissue had been subjected to previous freeze-thaw cycles. Geometric analysis In order to understand geometric/structural contributions to the mechanical performance of billfish rostra. Histology In order to investigate the tissues comprising the rostra. with a digital camera (Leica DFC 420c Wetzlar. Wetzlar. I applied beam theory analyses to transverse sections of the rostra of four 14 . Germany). Samples were observed under compound microscope (Leica CTR 6500 Wetzlar. 50 % H20) -sodium citrate (500 g NaH2C6H5O7. The use of all tissue samples was approved under the University of South Florida Institutional Animal Care and Use Committee. which may compromise bone tissue and cellular ultrastructure (e. Germany). 2500 ml H20). Andrade et al. 50 and 100x. Germany) and stained using hematoxylin and eosin. Whole skull scans were rendered for figure purposes were performed in Mimics software (Materialise HQ.g.

Germany) by first digitally isolating the rostrum (by cropping out all tissue caudal to the nares). the slice containing the rostral tip represented 0% length. analyses of cross-sectional geometry in MATLAB (see below) produced nearly identical trends. where the grayscale thresholding range was set at the start of the MATLAB script through an iterative series of threshold steps on individual original (full grayscale range) CT slices.swordfish and two blue marlins (Table 2. to extract the bony tissue. Berlin.g.e.3) using a custom design MATLAB script (written by Mason Dean. when thresholding methods were compared for the same CT datasets. However. The rostrum includes a range of tissue types (e. adipose tissue). Rostral bone was isolated within each dataset using the Segmentation Editor in Amira (Mercury Computer Systems. cartilage. Slices were then selected at intervals of 2% element 15 .e. bone. and then made small-scale adjustments to the selection range while noting the effect on the morphological accuracy of the resultant volume (i. This “bone selection” method resulted in more morphologically accurate volumes than an alternate method. beginning by normalizing rostrocaudal positions to percent lengths to facilitate comparison across scans (i. whether the volume represented more or less bone than was known from dissection to be there). indicating technique robust. regardless of thresholding method Each resultant thresholded (i.e. The script then performed a slice-wise analysis of cross-sectional geometry. “bone-only”) volume was sectioned orthogonal to the longitudinal axis of the rostrum and an image stack of cross-sections exported to the MATLAB script. These analyses were restricted to the contribution of hard tissue (bone) as CT scanning captures only bone structure accurately and bone occupies the majority of the rostra. I selected the largest peak from the scan’s histogram distribution of grayscale values. used with permission see Appendix) utilized with permission of Mason Dean) described below. the slice containing the caudal end of the rostrum represented 100% length).

2002). The standard integral typically used to describe well defined geometries (circles. The above 16 . and d is the perpendicular distance from the NA (NA was determined as the axis perpendicular to the applied force passing through the centroid of each cross section). (A). cross-sectional area. the second moment of area of about a given neutral axis (INA) is calculated with the following equation: ? ??? = ∑(???? + ???? ? 2 ) (1) where n is the number of individual pixels.length. For each of the 51 slices per rostrum. assumes infinitesimal area elements (Gere 2002). the script converted the grayscale “bone-only” images to binary images (white = bone. the analysis was simplify by focusing only on the bone tissue and assuming it has a consistent modulus down the length of the rostrum and between species. However. black = soft tissue and voids) and analyzed the distribution of white pixels around the cross-section’s centroid in order to determine a series of variables describing rostrum cross-section geometry: second moment of area. I. and is therefore indicative of resistance to bending. Apix is the pixel area. the area of the element cross-section with any holes/internal black pixels converted to white pixels) (Fig. Second moment of area describes the distribution of material around a neutral axis (NA) in a cross-section and perpendicular to the line of applied force. squares). and filled-CSA (Af.1). 2. Ipix is the second moment of area of each pixel (relative to its own centroid). as the non-bony tissues are located closer to the NA and their moduli are as of yet unknown (although likely orders of magnitude less). which can be accounted for by scaling the contribution of each tissue according to its Young’s modulus (Gere. this selection interval was determined via sensitivity analysis to provide a balance of resolution of data trends and script efficiency. For each “cross-section”. Billfish rostra contain multiple tissues with different material properties.

indicating a greater resistance to bending along one axis. respectively (see “cross-sections” in Fig. describing the anisotropy of bending resistance for the cross-section. where area elements (pixels) have finite areas. Whereas an ellipse would exhibit a higher ratio. The major and minor axes are defined as the longest and shortest diameters of the cross-section.1). as the second moment of area of asymmetrical sections can vary with the chosen bending axis —evidenced by the example of an architectural I-beam with a higher second moment of area when bent in line with its longer cross-sectional axis—second moment of area was calculated for bending in line with the major axis (Imaj) and the bending in line with the minor axis (Imin) of each cross-section. these values are only meaningful as relative measurements and so are presented as percentages of each scan’s maximum value. in both species. using imaging phantoms of varying hydroxyapatite composition). 17 . indicating isotropy in bending resistance. a circle’s moment ratio would be 1. from 0-100%. However. As the scans were not calibrated to materials of known mineral density (e. these structural axes correspond to the lateromedial and dorsoventral axes of the rostra. A) per cross-section relative to that of the hypothetical filled “cross-section” (Af): %??? = ?/?? (2) In addition the relative mineral content per “cross-section” was estimated by calculating the average grayscale value of mineralized tissue. The ratio of the two moments (Imaj/Imin) is a mechanical aspect ratio. 2.g.equation is better suited for (pixelated) CT data. The cross-section was further described as the distribution of material by calculating the proportion of bone (number of white pixels.0.

Bending experiments in a material testing system (MTS)

Billfish heads were thawed and prepared for material testing by removing all soft tissues

from the skull. Once cleaned, each skull (neurocranium) was potted in fast curing cement

(Rockite, Hartline products, Cleveland, OH, USA), firmly encasing the head while leaving the

entire rostrum exposed, simulating a cantilever beam. The embedded skull was then anchored to

the floor via a holding device (Fig. 2.2) and the tip of the rostrum fixed to the crosshead of a

materials testing device. The attachment point of the MTS was located approximately 15% of the

rostrum length from the tip, representing a loading point (LP) that might be expected during prey

contact. To determine the reaction of tissue along the length of the rostrum to distal loads, four

transverse regions were demarcated (areas 1 through 4, distal to proximal), starting at 30%

rostrum length and spaced approximately 20% apart (these relative positions represented the best

locations to survey strain along the majority of the rostrum accounting for differences in length

in both species). Each area was fitted with six strain gauges oriented parallel to the longitudinal

axes of the rostrum (C2A-13-125LW-120, Vishay Measurements Group, Inc. Raleigh, NC,

USA): four on the dorsal surface (two lateral and two medial) and two on the medial ventral

surface (Fig. 2.2). For proper strain gauge attachment, each region was smoothed with 400-

grade sandpaper, and excess oil removed with acetone. Strain gauges were glued to the

underlying bone with Mbond glue (Vishay Measurements Group, Inc. Raleigh, NC, USA).

Because some of the skeletal elements at the base of the most proximal portion of the rostrum in

blue marlin (area 4) are supported medially by soft tissue, and removing them could greatly

affect the structural integrity of the rostrum, strain gauges could not be attached here, decreasing

the total number of strain gauges for this species to 22.

18

Because the location of the NA depends on load orientation, different strain gauges were

selected for the two different loading regimes utilized (lateral and dorsoventral). For example,

only strain gauges located on the lateral edges of the rostrum were analyzed during lateral

loading (Fig. 2.2). Due to the lack of knowledge of rostral bending during normal feeding

behaviors in billfish and the limitations of the MTS system, displacements were fixed to ±1 cm

for all bending tests. Each rostrum was loaded under displacement control at the same loading

point with a 50 lb load cell (JP 50, Honeywell, Golden Valley, MN, USA) at a frequency of 2 Hz

in a material testing system, this was the maximum frequency allowed by the system, since

higher values resulted in vibration interference (MTS System Corporation, Minneapolis, MN,

USA). Loading tests were conducted in dorsoventral and lateral planes to simulate likely striking

directions, with data (strains, cross-head displacement and measured force) recorded at 1000 Hz

in a Megadac data collection system (Optim electronics corporation Germantown, MD, USA)

Using beam theory the following variables were estimated for each of the four areas on

each rostrum. Stress was calculated using the following equation,

? = ??/? (3)

where M is the bending moment at each area calculated by multiplying the maximum measured

load from each bending regime by the distance from the loading point to each position where

most strain gauges were aligned for each area; at a given position, d, y is the in-plane distance

from the NA to each strain gauge at that location (Fig. 2.2); and I is the second moment of area

associated to each NA (mm4). For each area’s “cross-section”, I and y were calculated in

MATLAB; for the latter, physical measurements of the distances of strain gauges from the lateral

edge of the rostrum were used to determine their dorsoventral positions in each digital “cross-

section”, and the dorsoventral distance y of those points from the neutral axis. Since we were

19

interested in estimating the maximum stress generated by the rostrum during a set displacement,

stress was calculated utilizing the largest bending moment at each area for each experiment

(made by the product of the largest load and the distance from the strain gauges at each area to

the loading point). Although the stress formula has been formulated based on simple structures in

engineering, it has been widely used in biological systems, however, caution should be taken at

interpreting its results since some deviation from its original assumptions may apply (i.e. the

rostra do not have a constant cross sectional area).

Using the stress calculated above, Young’s modulus was calculated to estimate the

material stiffness at each strain gauge location using the following equation:

? = ?/? (4)

where ɛ is the strain gathered from strain gauges at the maximum bending moment (estimating E

by this method assumes that the material is linearly elastic, however, similar values of E, derived

from the slope of stress-strain curves, were reported for several billfish species by Atkins et al.

(2014), supporting this results). Flexural stiffness (GPa*mm4) was calculated:

???????? ????????? = ? × ? (5)

where E is Young’s modulus and I is the second moment of area previously calculated. This

parameter estimates the resistance to bending of the rostrum at all areas, allowing an integrated

understanding of material properties and responses to load along the length of the rostrum.

Biological loading scenarios: Point loading and hydrodynamic loading

In addition to the geometric analyses above, we used a second MATLAB script (written by John

Dunlop, used with permission see Appendix) to examine the effects of cross-sectional form on

rostral stresses for both species for two possible loading conditions: point-loading (a single/point

20

the observed cross-section’s rostrocaudal distance from the loading point (i. stresses were calculated along the length of the rostrum for two loading directions: simulating the rostrum moving laterally (i. with both species’ rostra scaled to 700 mm tip-to-base length to allow a length-independent. ?max_ ?? ???? = (6) ???? (?) ???? (?) Maximum normal stress is a function of the applied load. in line with the rostrum’s cross-sectional major axis) and moving dorsoventrally (i. resulting from the rostrum being swiped through the water) (Fig.e.load. equivalent to the billfish striking a prey item with the tip of the rostrum) and hydrodynamic loading (a load along the full length of the rostrum. determined as described in the Methods and rescaled to a rostrum length of 700 mm).e. hydrodynamic loading). Rostrum cross-section dimensions were determined from CT scan data (see methods above). respectively. 2. F. and the second moment of area for that loading direction (Imaj or Imin. Stresses were calculated using equations for beam bending with the assumption of small deformations. x.e. distance from the tip of the rostrum). interspecies comparison. 2002): ??? ??? ?max_ ??? ???? = .3). this can be thought of as the maximum stress experienced by a point on the surface of a cross-section that is furthest from the neutral axis in a particular loading orientation (Gere. we first calculated maximum normal stresses for rostrum cross-sections: since the highest stresses will be experienced on the surface of the rostrum. in line with the rostrum’s cross-sectional minor axis). a linear dimension of the cross-section in line with the applied load: b = one-half major axis length for lateral loading or a = one-half minor axis length for dorsoventral loading. For each loading scenario (tip-loading vs. Maximum stresses resulting from tip- 21 . For tip-loading.

and therefore the shape which. we selected a cross-sectional shape that could act as a proxy for actual rostral morphology. the elliptical and diamond cross-sections were as wide and tall as the rostrum itself at any given tip-to-base location). by comparing the maximum stress profiles for tip-loading for actual rostrum morphologies (see previous paragraph) with maximum stress profiles for hypothetical rostra with elliptical or diamond-shaped cross-sections. The aspect ratios for these idealized cross-sections were the same as those for the biological sections (i. 6 to calculate maximum stresses per cross-section. First considering movement in a 22 .loading were calculated at 2% distance-increments from the tip to the base of the rostrum for both species and for both lateral and dorsoventral loading. 1965. CD ( x ) . these dimensions were used to calculate I along the length of the hypothetical bill using available equations for ellipses and diamonds (Gere. moving through water with subcritical Reynolds numbers (laminar flow) (Hoerner..e. This allowed determination of the simplified cross-sectional shape that most accurately approximated stresses calculated for actual rostra. We assumed a simple elliptical cross-section with the linear cross-sectional dimensions (i.e. 2012). 2012) and these values were used in Eqn. As the following calculations of hydrodynamic loading stresses are simplified considerably by using symmetrical geometric cross-sections. McHenry et al. a dimensionless number expressing the drag of a given cross-sectional shape in a moving fluid. b and a respectively) of the actual rostrum (see previous paragraph). The calculation of stresses resulting from hydrodynamic loading first required the determination of a drag coefficient. was most mechanically similar to actual rostra. major and minor axis lengths. The elliptical cross-section proved to be the more accurate approximation of both species’ cross-sectional profiles and so was used for the subsequent hydrodynamic loading calculations. for these purposes.

020 kg•m3) equivalent to 20°C seawater (Denny.015 + 1. 1993).e. The shear forces. with the medium’s density. at 2% increments down the length of the rostrum). We assumed the rostrum tip was swung through the water around the base with a velocity of 1m•s-1. r (1.direction parallel to the major axis of the cross-sections (i. lateral movement of the rostrum). V ( x ) .e. in the rostrum counter-acting the drag forces imparted by the moving fluid were then calculated by integrating the drag forces along the rostrum: ? ?(?) = ∫ ? (?)?? (9) 0 These shear forces were then integrated along the rostrum’s length to determine the moments acting along the rostrum as a result of the structural response to drag forces: ? ?(?) = ∫ ? (?)?? (10) 0 The calculated moments were then used to determine the maximum hydrodynamic loading stresses experienced by a cross-section: ℎ?? ?(?)? ???? = (11) ?(?) 23 . the drag coefficient can be calculated by: ?(?) ?(?) ?? (?) = 0. The drag force per unit length for motion in the lateral direction as a function of length is: ?(?) = ?? (?)?2?(?)?(?)2 (8) for dorsoventral motion the same equation applies with b ( x ) replacing a ( x ) .1 (7) ?(?) ?(?) Calculated drag coefficients were then used to determine the forces resulting from drag acting on each portion of the rostrum (i.

Although the majority of the adipose tissue was found in area 4. (7-10). a descriptor of 24 .e. 2. particularly in area 4. F. allowing determination of a maximum hydrodynamic stress profile for both species and in two loading directions. for dorsoventral rotation of the rostrum (i. indicating that the observed species- specific morphologies have mechanical consequences. hydrodynamic stresses were calculated at 2% increments along the bill. Three main tissues were observed: acellular bone (a bone lacking osteocytes. Second moment of area (I. adipose tissue and hyaline cartilage become more dominant. Fig. motion parallel to the minor axis of the cross-sections). 2. F) and acellular bone is relegated to the periphery.4. this tissue was also observed intermittently in smaller quantities within canals present throughout the acellular bone of the rostrum.5E.4E. 2. 2. a ( x ) was exchanged for b ( x ) and vice versa in Eqns. where they comprise most of the center of the “cross- section” (Fig.4A-D.As with the tip-loading regime. 2012). Moving proximally towards the base of the rostrum.5). 2. Results Histology The rostra of both species are composed of similar tissue types that appear to be arranged in similar patterns along the length of the rostra (Fig. Geometric analysis Swordfish and blue marlin exhibited diagnostic differences for most of the variables in the CT-scan based analysis of cross-sectional geometry. Fig. and hyaline cartilage. The primary component of distal cross-sections (Fig.5A-D) was acellular bone. adipose tissue. with proportions of the tissues changing in distinct ways from tip to base. Cohen et al. 2..

bone forms only a thin peripheral layer but is arranged far from the neutral axis. as a function of the dissimilar cross-sectional shapes of the species’ rostra.4- 2. 2. whereas the pattern of 25 . Swordfish rostra are extremely asymmetric in morphology and in the contribution of rostrum shape to bending resistance. in swordfish the proportion of mineralized tissue shows jagged oscillation distally. 2.6A). reflecting the periodic bony chambers within the distal rostrum (Fig. which show a proximal decrease in bone and increase in adipose tissue and cartilage (Figs. resulting in a high I for a comparatively small amount of bone tissue. representing a solid bony rostrum. This ratio is greatest distally and decreases proximally as the rostrum deepens closer to the head (Fig.5). Both species show a proximal-to- distal increase in the mean relative bone mineral density of the rostra. 2. D).the cross-sectional distribution of material in the direction of loading and a proxy for bending resistance) increased proximally in both species and in both principle loading directions. with I in lateral bending ~10-16 times greater than that for dorsoventral bending.6C. the ratio of I for loading in the dorsoventral and lateral directions (Imaj/Imin) differed considerably between species. In proximal regions of the rostrum. 2. However. This is reflected in the abrupt proximal (~ 75-80% BL) decrease in the proportion of mineralized tissue in each “cross-section” (Figs. indicating a more uniform distribution of material and isotropic bending resistance (Fig.6B. 2. where the rostrum begins to merge with the head region. In blue marlin I was only slightly greater for loading in the lateral direction. and the ratio of Imaj/Imin was fairly constant along the length of the rostrum (~2-3). as well as in the histological data. particularly at ~75-80% bill length (BL). Table 2.1). Whereas in blue marlin the proportion of mineralized tissue in “cross-sections” is approximately 100% in distal sections (< ~80% BL).6C).

the average maximum stress distribution did not vary much along the swordfish rostrum.6 N/mm2 (areas 1-4 respectively). Although similar trends in E were observed for the blue marlin. 2.6C. During lateral loading.3 GPa calculated in lateral loading (areas 1-4 respectively).9 N/mm2 (Fig.1 GPa when calculated in dorsoventral loading (Fig.8 to 3. Similarly. For the blue marlin. both species showed an approximately similar distal-to-proximal trend of slight increase in stress from area 1 to 2 and then a gradual decrease to area 4.decrease in swordfish is more gradual. and that of blue marlin is consistent until approximately 70% BL and then decreases more sharply (Figs.7 to 9. ranging from 14. the average maximum stress distribution during lateral loading ranged from 7.5 to 3. Fig.2 to 5.1 to 1.7A). and area 4 decreased to 4. Young’s modulus. and from 12. 2.9 N/mm2 (areas 1-4 respectively) with stress in the three most distal areas being considerably greater than that in the most proximal area 4.9 to 3. E. In the swordfish.7B). 2.7C). 2.2 N/mm2. D). values tended to be larger. decreased proximally from 12.5 GPa in lateral loading and from 16. ranging from 1. 26 . with blue marlin stresses being two to four times higher.3 N/mm2 (areas 1-4 respectively. Although the magnitude of stresses in the rostra of the two species were considerably different. the stress distribution was higher along the rostrum ranging from 2.4 to 5. During dorsoventral loading.4 to 1.7D). 2. the stress distribution in the three distal areas ranged from 8. during dorsoventral loading.7 GPa in dorsoventral loading (Fig. Bending experiments in a material testing system (MTS) Stresses along the rostrum were calculated as a function of rostral geometry and load during bending experiments where rostra tips were displaced +/-1cm.

2.7E). During lateral loading EI ranged from 4.3 106 GPa mm4 (Fig.9 104 to 1. Therefore. Flexural stiffness also increased proximally in the blue marlin. although values between the two loading planes were more similar than those of the swordfish. 27 . swordfish rostra showed almost three times greater stresses (Table 2. determined the corresponding stresses resulting from a similar moment value in both blue marlin specimens.6 x 105 GPa mm4) and dorsoventral loading (2.0 N and 123. However. which was considerably lower.2 105 GPa mm4) (Fig.7F). which accounts for both material and geometric contributions to bending resistance. B). The use of the swordfish maximum moment as a reference value for both species was preferred over load standardizations (standardizing the values to similar loads for each species) to account for small differences in the position of the strain gauges between species because bending moment calculations take into account both load and distance from load.9 N compared to the swordfish 19. (For the full range of values see appendix 1) It took considerably larger loads to displace the blue marlin rostrum the same fixed distance (±1 cm) as that of the swordfish (maximum loads applied to the blue marlin rostrum were 173. Flexural stiffness. especially for the distal half of the rostrum.3 N and 7. as opposed to the responses to the same maximum displacement. This “standardized” stress allowed us to illustrate the difference in the species’ tissue stress responses to the same moment. rather than comparing stresses resulting from both species’ maximum loads. increased proximally in the swordfish during lateral (3. 2.4 105 to 1.0 106 GPa mm4 and dorsoventrally from 2. I determined the largest moment value during the swordfish experiments. Results from standardized moments showed similar stress values for both species during lateral loading with the exception of area 4 for blue marlin. lateral and dorsoventral loading.8A.2. during dorsoventral loading. respectively).1 N.2 105 to 2. and then for each strain gauge. 2. Fig.7 x 105 to 9.

C). the swordfish rostrum appears suited for use as a light-weight. uniaxial weapon.g.Biological loading scenarios: Point loading and hydrodynamic loading For a hypothetical point loading scenario. Simulations of hydrodynamic loading during head swinging indicated that swordfish experience the highest maximum stress and drag during dorsoventral loading and lowest maximum stress and drag during lateral loading. with blue marlin values being intermediate for both variables in both loading directions(Fig. both rostra show opposing trends in I and E. with the former increasing rapidly proximally. 2. Discussion Results from this study suggest that the morphological differences observed between swordfish and blue marlin rostra have performance implications.9A).9B. diminishing towards the base (Fig. swordfish had higher stress values along the rostrum in both loading planes compared to blue marlin (Fig. Despite the cross-sectional shape differences between the two species. the results show several material and structural commonalities between blue marlin and swordfish rostra. use in feeding) may have shaped rostral anatomy in both species. solid javelin with cross-sectional anatomy suggesting multi-axial use. 2. the blue marlin rostrum is built like a short. and that these morphological and mechanical differences may be consistent with different feeding behaviors. D). Stresses calculated for the swordfish rostrum during dorsoventral loading were considerably larger than those for lateral loading. low drag.7C. in contrast.9A). The decrease in E proximally means that the increase in EI must solely result from disproportionate 28 . growth. 2. In general. but the latter increasing distally (Fig. Considering the possible role of the rostrum during feeding. providing strong evidence that common pressures (e. Stress values for blue marlin were lower and very similar for both loading planes. 2.

but also the peripheral arrangement of bone in this area. compensating for the increase in bending moment (Currey. 2004. Stress values in the tissue resulting from the bending experiments were shown to be approximately similar among the distal regions (areas 1-3) for both species (Fig. Horton and Summers. 2. likely explaining the consistent stresses in the distal regions. porcupine quills. Meyers. D).6). achievable due to the comparatively large I values at the base (>60% bill length). 2. perhaps explaining the observed stiffness gradient. 2. 2. as E and mineral density are positively associated in a variety of mineralized tissues (Currey.4. The distribution of grayscale intensity in rostrum CT scans suggests that bone mineral density increases distally in the rostrum in both species (Fig. et al. Magwene and Socha. and feather shafts (Bonser. 1984). Biological structures that have a similar conformation (solid exterior and a softer. 2. 2013) have been suggested to not only increase I in a structure but also to decrease the probability of local buckling by dissipating fracture energy and preventing the collapse of the thin cortical walls. This increase in I is a function of the change in geometry and the large cross-sectional areas in proximal regions. Gudger (1940) 29 . Furthermore. while also minimizing weight (Ma et al.. 2013). 2013). 2005.5. Meyers. A strategy to keep stress constant along the length of a cantilever beam is to increase the cross- sectional area towards the fixed end.changes in I. 2001.4A.6C. light-weight interior) such as the toucan beak. Fig. Stress values tended to be comparatively low in area 4. Billfish rostral cross-sectional area and I increase proximally (Figs. area 4).4-2. 2009. 2008. This arrangement allows for a high I without necessitating increased weight. Seki. as the core of the base of the rostrum is filled with low density materials (adipose tissue and cartilage) that are lighter than a comparable rostrum of solid bone (Fig. B).

. the relatively smooth and elongated rostrum of billfishes may reduce water disturbance. 2001).proposed this filling in billfishes may also act as shock absorber. squid beaks (Miserez et al. In addition. The ecological implications of the distal increase in material stiffness may be associated with feeding.. Previous work has shown that the drag experienced during lateral swiping of the elongate rostrum in alligators is proportional to the height of the jaws (McHenry et al. similar to billfish rostra . as this change minimizes deflection of the distal portion of the rostrum and provides a hard surface for striking prey. remodeling (Atkins et al. Additionally. 2006). suggest the tissue is under regular loading and therefore more prone to damage and consequently. thereby delaying detection of approaching billfish by 30 . Distal stiffening of rostral material could also counteract structural tapering relating to hydrodynamic demands. Billfish rostra are subject to periodic loadings over long periods of time. since the bow wave generated by a predator can be detected by prey (Visser. 2009) and spider fangs (Politi et al. distal stiffening of the rostrum may ultimately be a strategy for maintaining adequate flexural stiffness in areas where I is selected to be comparatively low for hydrodynamic reasons. 1980. While minimizing element height (via distal tapering) may reduce drag in billfish rostra. which may result in fatigue damage and favor the formation of microcracks in this stiffer area. 1984). Similar gradients of stiffness have been reported in other biological structures including bird feathers (Macleod. the higher incidence of remodeled bone morphology in the distal region of the rostrum. dampening vibrations during striking of prey... 2014). Bonser and Purslow. 2006). as in bone and nacre (Currey. however it also comes at the cost of potentially reducing cross-sectional area and resistance to bending (McHenry et al.. 1995). the latter two systems also acting as predatory weapon. 2012).

prey. Generalized patterns of stress. The lower values of stress at the base of rostrum also coincide with a region of multiple sutures. 2003. Krauss et al. due to the proximal increase in I. more mineral dense. 2006. All of these factors may decrease the likelihood of failure at this region. and also preventing damage to a region of higher vascularization and growth. 2000. Sutures have been found to influence patterns of stress and strain by resisting or allowing deformations depending on load orientation and/or magnitude (Rafferty et al. 2002. second moment of area. and where the rostrum connects to the rest of the head (Fig. in addition to that in an ongoing investigation of billfish tissue morphology (Atkins et al. Evidence from the histology and mineral density gradient of the rostrum found in this study... Basal regions of the rostrum (i. suggested growth zones) are prone to less stress and. and more remodeled. material stiffness. 2. EI was also increased. Markey et al.10). preventing the compromise of vital organs such as the nares.. where multiple cranial bones converge. Sun et al. 2009) but also can act as bone deposition sites in mammals (Opperman. indicate that distal regions of the billfish rostrum are less porous.. 2014). McHenry et al. This suggests that distal areas may contain older tissue than basal regions and therefore that the rostrum in billfishes may grow from its base by “pushing” older material distally (although rostrum development is not fully understood and other factors such as mechanical demands may play a role in its development). Coincidentally. as suggested for other vertebrates with long jaws including water snakes and alligators (Alfaro.e. and flexural stiffness in both billfish rostra seem to follow a common pattern that may aid in overcoming conflicting demands imposed by the rostrum’s function and shape.. 2006). rostra in several different billfish 31 . 2004) and so may provide free surfaces for growth and bone deposition in billfish rostra.

2. Drag forces. B). 1994.species have been more often documented to show breaks in their distal halves (Frazier et al. While I was approximately equal for both species during lateral loading (Fig. surface characteristics.9 GPa swordfish and 16. as compared to the swordfish (Imaj/ Imin > 8. Additionally. 1996.4 GPa blue marlin) agree with those determined in a different study for five billfish species (including those studied here) using material testing techniques (E ranged between 12-20 GPa.48 GPa.20 GPa. for example. Horton and Summers. 1997). are influenced by a structure’s shape.. such as great sculpin. 2014) but also exceed the values found in other acellular boned fishes. 2.6A. Cohen et al.7C.. 2012). stiffness values calculated from distal strain gauge data (area 1. Moreover values of stiffness in billfish are not only shown to be higher than most values reported for other fish but also to be closer to values reported for mammals (Atkins et al. Fierstine et. speed of movement. 2012) as well as those with cellular bone found in the common carp.0) (Fig. Atkins et al. Mechanical demands associated with feeding may not be the only factors dictating shape differences between species. Overall.0) due to its almost circular cross-section. the blue marlin rostrum showed higher I during dorsoventral loading and greater equivalence of bending resistance between lateral and dorsoventral loading (Imaj/ Imin ~ 1.. Myoxocephalus polyacanthocephalus (6. D) and E varied with respect to loading regime in swordfish. blue marlin rostra showed E values higher than those for swordfish for most of the regions along the rostrum (Fig.. Fierstine and Crimment.6A. Cyprinus carpio (8.. B). Cohen et al. 2009) and tilapia Oreochromis aureus (7.51 GPa. al. 2014). their morphological differences revealed mechanical disparities that suggest different feeding behaviors. suggesting material heterogeneity in this species. and the surrounding fluid’s density and viscosity 32 . 12. 2. Although broad structural similarities clearly exist between rostra of these species.

facilitating low-resistance. 2. I. 33 .(Vogel. reducing pressure drag (Vogel. Rod-like structures are suited to withstand loading in multiple directions. E. whereas elliptical cross-sectional beams.9C) due to the depressed lenticular form of the rostrum. similar to the multi-plane striking behavior observed during feeding in sailfish (Domenici et al. 2003). however. lateral swiping at its prey. this support for differences in rostrum motion during striking are also suggested by differences in vertebral morphology between the two species. Consequently swordfish may be limited in the extent to which they can use dorsoventral striking. 2000. (1990) found that the flexibility of the blue marlin vertebral column increased when the zygaphophyses were removed. Results from modeled biological loading scenarios indicate that drag forces and stress are greater in swordfish during dorsoventral hydrodynamic loading than in blue marlin. 2003).. 2014). In contrast. as streamlined shapes delay flow separation. are better designed to withstand loading in a single plane (Etnier and Vogel. Patterns of σ. as Hebrank et al. and therefore drag forces acting on the rostra can conceivably influence both feeding and hydrodynamics at the same time. Swordfish rostra. the lack of zygapophyses in swordfish may allow extensive lateral flexibility of their body. EI and theoretical drag calculations suggest that blue marlin may have a rostrum better suited to strike its prey in a wider range of motions. which incurs 40-times the drag forces compared to lateral striking (Fig. 1990). The potentially greater lateral flexibility of the swordfish body may be related to the dorsoventral depression of the rostrum and its reduced hydrodynamic drag in the horizontal plane. a species with a rostrum similar in shape to that of the blue marlin. 2.9C). such as the swordfish rostrum. Interestingly.. would exhibit the lowest drag forces during lateral loading (Fig. The vertebral column of the blue marlin is reinforced with zygapophyses that provide reinforcement and stability but decrease flexibility (Hebrank et al.

gut contents of swordfish showed prey being severed which may be due to the lateral swiping of the sharp.. S C. 2. Nakamura. References Andrade M. Aleyev. but its design. and material properties favor its role in prey capture. 1985).Currey. Nekton. 2002). Sa. 1985. Stillwell and Kohler. 1968. The Hague.M.G. 279-287. ventral.B. whereas swordfish rostra seem to be highly specialized for lateral striking due to the arrangement of skeletal material in a way that maximizes lateral bending resistance while decreasing drag.S. despite the differences found between these species there are still many variables converging into similar patterns that may explain how to build an efficient biological beam that can act as a weapon in multiple ways. Whether this structure evolved as an adaptation for feeding remains uncertain.11A) support the theory of multi-directional striking in istiophorids. Junk. tissue architecture. 9. 2007) and pictures of sailfish prey bearing injury on differing regions of the body (Fig. do. 204-215. Forward attack modes of aquatic feeding water snakes. T. N. A. Prey fishes in the stomach contents of blue marlin showing lacerations to the dorsal. Cell Tiss. Marchionni. (2008).. blue marlin rostra are stiffer and better suited to strike prey in multiple planes. 1985) (Fig. and Sadigursky. (1977). lenticular rostrum of (Goode. E. Bank.T. de Bittencourt. 2. Func..G.11B).C. Ecol. 16. Alfaro. Effects of freezing on bone histological morphology. In contrast. C. M. 1883. Y. and caudal body regions (Shimose. Stillwell and Kohler. M. However. 34 . (2002). Injuries to prey provide insight into billfish feeding behavior (Scott and Tibbo. In conclusion.

New Zealand Massey Univ. J.J. M. The stimulus for escape. (1984). Monsonego-Ornan. (1993).K. R. J. Abh. A. 20. (1974). Oxford Univ. M. 941-942. Mat. Princeton. Comparison of structural. Atkins. Dill.. The escape response of zebra danio (Brachydanio rerio). Bones: Structure and Mechanics. (2002).. PNAS. M. Currey. Davie. Let. architectural and mechanical aspects of cellular and acellular bone in two teleost fish. Princeton.1412372111. Dean. Biol. Dean. (2014). R. Press. J.H. Behav.A. and Shahar. (2012). Palaeontol. L.. P. Pacific Marlins: Anatomy and Physiology. The mechanical performance of medullary foam form feathers. NJ: Princeton University Press. doi/10. 710-721. 190.A. J. T. 1983-1993. E. Press. Biewener. Geol. NJ: Princeton Univ.. Sci. ed. The Mechanical Adaptations of Bone. Neues Jahrb. A. Anim.D.J.Atkins. P. 215. J. (1990). A.. 569-580. Shipov. Exp.. and Full. (1992). Palmerston North. J. Motta. 35 . Air and Water: The Biology and Physics of Life's Media. 279-297. R. Baumiller. A. Press. Theor. (1993). NJ: Princeton University Press. Biomechanics Structures and Systems: A Practical Approach.M. Remodeling of anosteocytic bone. Bonser. Denny. Crinoid stalks as cantilever beams and the nature of the stalk ligament. Princeton. Currey.D. Biewener. R. A. (2001). (2004).L. Oxford. Cohen. Incompatible mechanical properties in compact bone..1073/pnas. and Shahar. Habegger. M. Currey. L. Currey.D. J. 22. 231. Biol.

Fierstine. Etnier. Bull. Fierstine. 123-127. 72.. Fierstine. Couillaud. S. Proceedings of the International Billfish Symposium.D. (1996). (1997).. S. Sci. impaled by two species of billfishes (Teleostei: Istiophoridae). 205. Soc. 472-475.1098/rspb..2014.L. A. J. Kailua-Kona. Am. J. (1993). How sailfish use their bills to capture schooling prey. 1996. Hawaii. Reorientation of daffodil (Narcissus: Amaryllidacea) flowers in wind: drag reduction and torsional flexibility. H. H. Biol. (2000). Etnier. 36-46. The paleontology of billfish-the state of the art. The mechanics of the flower stem of the sedge Carex acutiformis.E. Herbert-Read. 495-499.0444. Fierstine. Proc.R.L. Contributed papers. Part 2. Proc.E.. Ed. Use of rostral characters for identifying adult billfishes (Teleostei: Perciformes: Istiophoridae and Xiphiidae). S... A paleontological review of three billfish families (Istiophoridae. August 1-5. and Crimmen. P. Marras. (1990). Viblanc.L. Bot. http://dx. Billfish Symposium. 9-12 August 1972. S. Pages 11-19 In R. Bull. Fierstine. Xiphiidae and Xiphiorhynchidae). (1996).. H.doi. A. S.J.E. Krause. and Krause. 1988. E. NOAA Technical Report NMFS SSRF-675 pp. 87. H. (1974). Wilson. 61.. P. (2003). and Vogel. Copeia 1996. Kurvers. Hawaii. An Atlantic Blue Marlin. 2nd Int.H. J. R. 148-161. Mar. S. P. Ann. 36 . Makaira nigricans. Ennos. Planning the future of billfishes. commonly cited examples of “swordfish” piercing wooden ships. Copeia. Kailua-Kona. and Voigt. Twisting and bending of biological beams: distribution of biological beams in a stiffness mechanospace. Bot. H. (2014).M.L. O. 281. Two erroneous. Steffensen. H.Domenici.L.L. N. Roy. 34-44.M. 29-32. Stroud.org/10. Review and contributed papers. Part 2.

M. (1940). J. 4256-4263. (2009). Mechanics of Materials. Stinson. (1977). 85-96.. Hoerner.F. Perciformes: Istiophoridae and Xiphiidae). Neveu.M. Anderson. Pitman. Block.M. Hiroyuki. S. Exp. Biol. Achaval.G. 216.W. Exp. H. Biol. J. 37 .E. Gere. D. J. 148. Huber. 449-459. I.R. Hebrank. Mechanical properties of sand tiger (Carcharias taurus) vertebrae in relation to spinal deformity. S. M. Env. S. J. Hebrank. Asiatic.R. M. and Prigioni..O. Koehl..C. Chelonia: Cheloniidae and Dermochelyidae) by billfishes (Osteichthyes.P. Mackie).A. G.. Long. 127-142. A. H... Beavers.R. J.. Shortfin Mako. Bengal Branch. Soc. F.L. and Summers.Fierstine. Makaira nigricans (Teleostei: Istiophoridae). 215-31. 1413-1420.A. J. R. Impalement of marine turtles (Reptilia. 212. Istiophoridae). J.. Isurus oxyrinchus.A.A. Biol. (2013). Koehl. 5 Ed. Y. Fluid-Dynamic Drag. D. (1997). J. (2002). (1990). Gudger. P. J. (1976). Mechanical organization of cantilever like sessile organism: sea anemonies. The allegated pugnacity of the swordfish and the spearfishes as shown by their attacks on vessels. 2. Horton. S. Exp. Plenum Publishing Corp.K.R..A. Fierstine. impaled by blue marlin.. Roy. Frazier. Mem.L. South. and Neer. Sci. C. 6. and Berzins. Hoerner Fluid Dynamics: Brick Town. M. Cailliet. Exp. E. Biol. Backbone mechanics of the blue marlin Makaira nigricans (Pisces.M. The material properties of acellular bone in a teleost fish.. J. Yamaguchi. NJ. Mechanical design in sea anemones. Bull. Biol. (1994). C.H.M. 3. (1965).H. Stamford. B. 117-121. Acad....L. Fish. CT: Brooks/Cole Publishing Co.A. 39. Calif. and Wainwright. In: Coelenterate Ecology and Behavior (Ed G.

D. Zool. J. Bion. Billfishes of The World. 255-396. P. Differential development of the rostrum and mandible of the swordfish (Xiphias gladius) during ontogeny and its possible functional significance.. W. (1988). Zool. 7. J.A. Macesic.J. No. 209. Exp. and Chen. 5. Biol. Publ. M. 87. (2013). McGowan. Makoto. J. (1985).. Ma. 65-71. 319. (2006). and Socha. C. P. Nohara. Can.. C. J.J. vol. Exp. Agen. Science 339.M. Kazuhiko. In vivo cranial suture function and suture morphology in the extant fish Polypterus: implications for inferring skull function in living and fossil fish. Res. Nobuaki.. Structural biological materials: critical mechanics-materials connections. Lab. and Summers.P. Hiroshi. S. D. 5. Bull. H. Biol. S. O. Exp. J.Nakamura. J. Flexural stiffness and composition of the batoid propterygium as predictors of punting ability. Fish.. M. Chen. Zhao. O. 66. (2003). Mechanical properties of contour feathers. Biological investigation on two types of bill internal structure of swordfish (Xiphias gladius) and genetic differentiation between the North and South Atlantic stocks.. (2013). Eng. I. J. 86-98. J. I. and Zhao.J. Main. Exp. McKittrick.. 1-65. N. FAO Species Catalogue. (1983). 38 . Magwene. Meyers. 28. 215. Elastic buckling of bionic cylindrical shells based on bamboo. A. R. L. Biol. Macleod.P and Marshall. 231-238. Synop. and Chow. Nakamura. 2085-2102. 1-13. J. Biol. L. K.125. (1980). 773-779. Motoki. Biomechanics of turtle shells: how whole shells fail in compression. FAO Fish. 496-503. Systematics of the billfishes (Xiphiidae and Istiophoridae). Seto Mar. Markey.. G. 2003-2012. (2008). (2012).R.

A. Science. C. P. Pippel. M. (2001). C. G. T. A spider's fang: How to design an injection needle using chitin‐based composite material.. K. J. C. Acad.R.. Dev. Eng. M. 44. 39 .. Trans.W and Marshall. and Rieqles. J. A.. 22. The biomechanics of the rostrum in crocodilians: a comparative analysis using finite element modeling. Biomechanics of the rostrum and the role of facial sutures.J.V. Rosario..R. W.W. Poplin. Politi. and Fratzl. 1816-1819. Exp. Chung. Daniel. S. 472-485. D.McHenry. 257-233. J. Opperman. 219.L.D. Mat. (1970). Biol. M. Swordfish and billfishes in the Atlantic Ocean. Miserez. J. McHenry. Hartmann.. L.T. Bai.M. S. Morph. Mishra. Adv... E. R. (2012). Ovchinnikov.. S. Meers..Y. S. Herring.V. 288.D. (2012).. Siegel. K. NOAA NMFS TT 71-50011. Quelques particularités anatomiques et histologiques du rostre de l’espadon (Xiphias gladius) L. P. and Herbertwaite. Schneberk. (1976). T. Y. Anat... Rafferty. Chengjum. Biomed. Ecology and functional morphology. and Patek. M. Barth.B.. 827-849. (2006). 1231-45. 29. F. Prog. Relationship between ultrastructure and nanoindentation properties of intramuscular herring bones. and Pharr. Sci. Li. P. Claverie. Poplin. Ann. C. (2003). Zaslansky. Func. Rec.. (2009).. 1082-1088.. 1105- 1108.. J. Dyn. Zok. and Pendharkar. 2519-2528. Isr. Priewasser.N. 215. Gearing for speed slows the predatory strike of a mantis shrimp.. C.. 319. A. V. F. F. (2000) Cranial sutures as intramembranous bone growth sites. 282. Rho.A.J. Sci. S. G. Ser. J. The transition from stiff to compliant materials in squid beaks. Clausen.

5281-5296. Shimose.W.N. Fish. (2007). M.0081323. T. Scott. Ecol. 468. Bd.1371/journal. around Yonaguni Island. 90-94. (2013). K. Saito. 215. F. (2008). Yokawa. Seki. Food and feeding ecology of the swordfish Xiphias gladius in the western North Atlantic Ocean with estimates of daily ration. Acta Mat.P. H. (1968). K. (1981). Van Der Elst. C. Visser. E. 222.. S. 420-422. and Meyers M..J. Herring. T. Y. Res. Schneider. Lee. during feeding. 150-161. 239-247. J. M. K. N... (2001). Cranial sutures and bones: growth and fusion in relation to masticatory strain.E. Hydromechanical signals in the plankton. W. and Roxburgh. 25. (2005). J. Ichthyol. M. Mar. (1964). 55. Res. R.H. A. southwestern Japan. PLoS ONE. Stillwell. Spearing behavior in feeding in the black marlin. Hydrodynamic characteristics of the sailfish (Istiophorus platypterus) and swordfish (Xiphias gladius) in gliding postures at their cruise speeds. (1985). Ichtyol.A.. Use of the bill during feeding in the black marlin (Makaira indica). S. and Kohler. Istioampax marlina. Mar.pone. 53.E. Anat.Sagong. Talbot. Yokawa. Evidence for the use of the bill by blue marlin (Makaira nigricans). Sun. and Tibbo. Seasonal occurrence and feeding habits of black marlin (Istiompax indica). and Tachihara. 1-24. Ser. and Tachihara.. Structure and mechanical properties of the toucan beak. K.. 903-972.. W-P. and Penrih. Food and feeding habits of swordfish. Jeon. Res. Xiphias gladius. Shimose. Copeia 1981. Copeia 1964. doi:10. in the Western North Atlantic.B. M. Part A 276. Prog. W. (2004). Choi. Canada.S. Ecol. 40 . Rec. Z.. Saito. 22. 54.

276..R. A. Dean. S. McHenry. 60-70..Vogel.. 12. P. Sci.A. Huber. and Summers. Clausen. Mechanical Design in Organisms. Is the spear of istiophorid fishes used in feeding? Pac. J. M... Wisner. Ferrara. Zool. Three-dimensional computer analysis of white shark jaw mechanics: how hard can a great white bite? J.M.N. Cunningham. Wainwright. Lowry. Comparative Biomechanics: Life’s Physical World. Currey. Princeton Univ. (2008). 336- 342. D.. 41 .. (1976). T. E. Moreno.P. R. K.. S. (2003).. NJ. J. and Gosline. Princeton: Princeton University Press. Biggs. C. S. Press.D. W.. Wroe.D. (1958). M. Princeton.

Second moment of area obtained from MATLAB geometrical analysis along the rostrum of two billfish species.1. swordfish (X. nigricans) 42 . gladius) and blue marlin (M.Table 2.

1 ± 0.7 ± 0.1 0.Table 2. Standardized values of stress obtained from bending experiments in blue marlin (M.2 BM LAT 1.2.3 ± 0.6 ± 0.0 ± 0.3 BM DV 0.0 0.3 1.0 ± 0.2 2.7 ± 0.4 ± 0.8 ± 0.3 ± 0.1 ± 0.3 SWF DV 2.3 0.2 1.2 1.6 ± 0.2 1. Standarized Stress (N/mm2) Area 1 Area 2 Area 3 Area 4 SWF LAT 1.4 ± 0.9 ± 0.7 ± 0.2 1.0 43 . nigricans).7 ± 0.1 1.3 1.2 2.

5 X.4 X.1 61. Species Lj-FL (cm) Weight (Kg) BL(cm) X. bill length was measured as the distance from the tip to the naris and is denoted as (BL) 44 . Meristic data from both species utilized in this study swordfish (X. nigricans (BM) 257.fork length (Lj-FL). Specimen information.3 37.2 77.5 59. gladius) and blue marlin (M.9 77.Table 2.1 72. gladius (SFW) 138.1 39. nigricans (BM) 257 172. gladius (SFW) 125 36. gladius (SFW) 146.7 Total length estimations in billfishes are commonly measured as lower jaw.8 147. nigricans).3.5 X.7 78 M.7 38. gladius (SFW) 147.5 M.

Binomial images were produced every 2% along the rostrum and the ratio of bending moments between two loading planes (Imaj/Imin).1. among other variables.Fig. were calculated and graphed along the rostrum. followed by binary images (black and white). Illustration of the cross-sectional shape differences between species and description of the major steps performed during the MATLAB geometric analysis. 45 . From top to bottom: complete skull renderings for both species (swordfish left and blue marlin right) followed by grayscale “bone-only” thresholded rostrum sections utilized for the analysis (number of “cross- sections” shown were reduced for space purposes). 2.

2. gladius) rostrum. 2. Outline of the apparatus settings for the bending experiments on the material testing system (MTS) during lateral loading on a swordfish (X. this is area 1) and y represents the distance from the neutral axis (NA) to one strain gauge on the dorsal surface of the cross-section. Note that although the calculation of d and y are shown here for only one strain gauge in area 1. Strain gauge (SG) location and areas along the rostrum are shown on the dorsal portion of the rostrum (from the most distal area. area 4).Fig. The complete layout of strain gauges can be observed within the dashed box showing a magnified representative cross-section of area 2. area 1 to the most proximal. 46 . these variables were calculated in each area (1-4). Some representative examples of variables utilized for the calculation of stress are shown where d represents the distance from the loading point to the area in question (in the figure.

hydrodynamic load scenarios in a swordfish (X.3.Fig. gladius) with dorsal and lateral views of suggested loading regimes. Simulated point load vs. 47 . A similar loading simulation was conducted for the blue marlin. . 2. B simulates the effect of water exerting a continuous load along the length of the rostrum (blue arrows) during lateral and dorsoventral movement of the head. A shows a point load simulating a lateral and dorsoventral load exerted by a prey item at the most distal portion of the rostrum (red arrow).

ventral on bottom. Upper surface of cross-section is the dorsal portion of the rostrum. 48 . Cross-section orientation: dorsal on top.Top image from left to right shows representative cross-sections from areas 1 to 4. 2.Fig. Images E and F show different tissues found on area 4 including cartilage and adipose tissue. nc = nutrient canals. Results from histological analysis performed along four regions of the rostrum of a swordfish (X. gladius).4. Images A-D show acellular bone present in all regions.

Upper surface of cross-section is the dorsal portion of the rostrum. ventral on bottom. Images E and F show different tissues found on area 4 such as cartilage and adipose tissue. nigricans). 2.5. 49 .Results from histological analysis performed along four regions of the rostrum of a blue marlin (M. Cross-section orientation: dorsal on top.Fig. nc = nutrient canals. Images A-D show acellular bone present in all regions (white areas around the edge of the rostrum in B and C show no tissue). Top image from left to right shows representative cross-sections from areas 1 to 4.

n=4) and blue marlin (M. C. mm4) blue lines show I about the dorsoventral plane (Imin) and red lines show I about the lateral plane (Imaj).6. the percent of cross-sectional area occupied by bone tissue (% mineralization) (blue lines) and the relative bone tissue grayscale values (a proxy for bone mineral density. A. D show. calculated relative to each CT scan’s maximum. 100 % = proximal base) of swordfish (X. B show second moment of area (I. green lines show the ratio between second moments of area (Imaj/Imin). n=2). nigricans) (left column.Fig. gladius) (right column. mean ± SE. red lines). 50 . Results from geometrical analysis along the length of the rostrum (0 % = distal tip. mean ± SE. 2. down the length of the rostrum.

Fig. D. lateral load) and (white dorsoventral load). 2. flexural stiffness (GPa*mm4). Young’s modulus (GPa). nigricans) on the right). swordfish (X. Intraspecific results from bending experiments in two loading planes (mean ± SE. B. gladius) values on the left and blue marlin (M. stress distribution along the rostrum (N/mm2). E. A. 51 .7. F. Black and white circles denote different loading orientations (black. C.

Fig. 52 . lateral plane and B.8. dorso-ventral plane (mean ± SE). Standardizations were performed in blue marlins (white circles) while swordfish values (black circles) where not modified. A. Interspecific comparisons of standardized stress (N/mm2) from bending experiment in two loading planes. 2.

red lines swordfish loaded dorsoventrally. Comparisons of localized and continuous loads among species and loading orientations. Rostrum length goes from 0 (most distal part) to 700 most proximal portion. B. blue lines are swordfish loaded laterally. A.Fig. load continuously applied along the rostrum. Stress applied at a localized point. 2. C. Each color represents a species with a particular loading plane.9. 53 . drag forces along the rostrum. green lines blue marlin loaded laterally and purple lines blue marlin loaded dorsoventrally.

Bones are individually labeled and colored. however. CT scan reconstruction of a swordfish (X. 1990) 54 . 2. the prenasal bone is still controversial for this species and is demarked with an question mark (see Fierstine. gladius) rostrum. Bone nomenclature follows Fierstine and Voigt (2006). the locations of the strain gauges are marked in area 4 to illustrate their arrangement in this highly sutured area on the proximal portion of the rostrum.10.Fig.

55 . Mexico. Since in both cases direct feeding events were not documented other types of feeding behavior may be equally viable. Decapitated squid from stomach contents of a swordfish suggesting possible lateral slashing used during feeding behavior (Photograph taken by Eduard Walker).Fig. 2. Arrows denote possible multiplane points of impact from the rostrum (Photograph taken by Rafael de la Parra). B. Injuries in prey items after a sailfish (Istiophorus albicans) feeding event in Isla Mujeres.11.

Stress distribution along each rostrum was constant. The blue marlin (Makaira nigricans) rostrum is mechanically suited for a wider range of slashing motions during feeding. Although the function of the rostrum is still in debate. logistical challenges associated with studying this enigmatic group have prevented questions regarding rostral function from being answered. Although the range of morphologies and sizes of this structure are suggestive of differential feeding behavior. Consequently. recent evidence suggests it is associated with feeding. the goal of this study is to assess the mechanical function of different rostral morphologies to ultimately infer feeding behavior in billfishes. Finite element analysis (FEA) is a mathematical technique that allows the determination of stress and strain patterns in morphologically complex structures and provides an excellent opportunity to investigate complex morphologies in logistically challenging groups. Patterns of von Mises stress and total strain energy suggest that distinct rostral morphologies may be functionally segregated. implying efficiency of 56 . CHAPTER THREE FEEDING BIOMECHANICS IN BILLFISHES: INVESTIGATING THE ROLE OF THE ROSTRUM THROUGH FINITE ELEMENT ANALYSIS Abstract Billfishes are a group of fish characterized by the extreme elongation of the upper jaw bones. whereas the swordfish (Xiphias gladius) lenticular rostrum is mechanically specialized for lateral swiping during prey capture.

Finally. 1970. The mechanical likelihood of other less commonly reported functions of this morphological novelty such as spearing of prey and hydrodynamic efficiency are discussed as well. 1997). Aleyev. This structure varies in size and shape among the 13 recognized billfish species. reaching up to 24% of body length. it has been suggested that the rostrum is used during feeding to injure prey that will be ultimately consumed (Scott and Tibbo. In addition. For example. however the greatest rostral disparity occurs between the families Xiphiidae and Istiophoridae. thereby resembling a sword. Xiphiidae). sailfishes and spearfishes) the rostrum is covered by villiform teeth. 1977. whereas other studies have suggested a drag-reducing hydrodynamic role (Wisner. Despite the conspicuous nature of the billfish rostrum. but see Sagong et al. 2014). The rostrum in swordfish (Xiphias gladius. prey including squid that were 57 . edentulous in adults. the function of this structure is still controversial. 1994). with a round cross section that also tapers distally (Gudger. Ovchinnikov. In istiophorids (marlins. Ovchinnikov.. Nakamura. 1958. and is relatively shorter than in xiphids.rostral function as a predatory weapon regardless of rostrum type. 2013). reaching lengths of up to 50 % of their body length. Introduction Billfishes are among the fastest and largest apex predators in the ocean. 1970. characterized by their most noticeable attribute. is long. and has a lenticular cross section with sharp edges that taper distally. Frazier et al. Fierstine et al. 1983). stomach contents and anecdotal observations corroborate species-specific feeding behaviors in billfishes. evidenced by the recovery of rostral fragments embedded in large predators such as sharks or other billfishes (Fierstine. 1997. 1940.. 1985. Stillwell and Kohler. an elongated bill or rostrum.. 1968. Some studies suggest that it has a defensive role.. this behavior that has recently been documented in the field for the Atlantic sailfish Istiophorus albicans (Domenici et al.

Rayfield. The application of engineering principles to biological systems. Fierstine. has provided a window into the investigation of feeding systems of large predators such as crocodiles. or biomechanics. This line of investigation has been particularly useful in the study of feeding behavior in extinct taxa such as dinosaurs (Rayfield. Chapter 2). 1988). 2007). 1996). Fierstine et al. 2001. This applies to systems that are difficult to 58 . and is particularly useful for the analysis of stress patterns in biological structures that are otherwise difficult to study in vivo (Rayfield 2007). or by a theoretical approaches such as beam theory and finite element analysis (FEA) to better understand stress patterns in biological structures (Richmond. McGowan. including slashing and spearing (Talbot and Penrith. 2007. Although indirect.. sharks.. injury patterns on prey indicate that istiophorids such as blue marlin may subdue their prey with a wider range of rostral motions. On the contrary. 2009). 1967. et al. inference of behavior from form-function complexes can be particularly useful in the investigation of experimentally intractable organisms such as billfish due to the predictive nature of morphology with regard to behavior (Koehl..severed into two or more pieces. However the lack of quantitative studies makes these assumptions speculative (but see Chapter 2). Many biomechanical studies focus on the understanding of how forces affect structures during their regular function. Shimose et al. 1962. 2009.. 2005.. Panagiotopoulou. 1997. and billfishes. indicating that these fishes may slash their prey with lateral swipes of the rostrum (Scott and Tibbo. Snively et al. have been found in swordfish stomachs. 2006). This can be addressed by experimental approaches such as the use of strain gauges to quantify material deformations. 1997. Finite element analysis is a noninvasive mathematical tool that creates computational models based on CT-scanned structures for which the distribution of stress and strain can be assessed. Huber et al. 2006. which would otherwise be difficult to address (McHenry et al.

the utilization of classical biomechanical approaches as means for validation is suggested (Richmond et al. 2005). beam theory.keep in laboratory conditions.. Using strain gauges. 2008. In addition. This may be due to its intuitive nature. 2010). and geometrical analysis. and even for extinct taxa (Rayfield et al.. since VM stress incorporates the three principal stresses associated to a 3D object into one variable that does not account for tension or compression (Moazen et al. those for which morphological complexity precludes experimental techniques. such as the localized information provided by strain gauges or the deviation from standard assumptions from beam theory. 2008. contributed to a better understanding of the evolution of reptile skulls (Moazen et al. 2009). 2005. FEA has aided in the elucidation of feeding behaviors in dinosaurs (Rayfield et al. Metzger et al. 2009). For example. Overcoming some of the common pitfalls from most utilized approaches in biomechanical studies. 2005...e.. Pierce et al. and has increased our understanding of craniofacial morphology and mechanical performance in mammals (Dumont et al. However since FEA is highly dependent on the accuracy of the models.. 2005).. The inference of feeding behavior from rostrum morphology was recently investigated in Chapter 2 for two billfish rostra with different morphologies. 2011).. 2012). it was determined that the rostral morphologies of swordfish and blue 59 . Cox et al. FEA has become more frequently used in the last decades (Panagiotopoulou.. Brassey et al. The most frequently reported variable in FEA studies is von Mises stress (VM). 2001). Finite element models can be interpreted through different variables such as stress (force per unit area) and strain (changes in length or deformation of a structure). Dumont et al.. VM stress is used as a proxy of bone failure (i. bone failure is estimated to occur when VM stress equals the yield strength of the material) (Keyak & Rossi 2000..

60 . one from a blue marlin (Makaira nigricans) and one from a swordfish (Xiphias gladius) were obtained from recreational fisheries off the Gulf of Mexico and preserved frozen until scans were performed. as this configuration may prevent stress concentrations leading to breakage. These species were selected due to the morphological disparity of their rostra and as representatives of the two billfish families. I will investigate whether billfish rostra maintain a constant stress distribution along their length in order to minimize the chance of failure at any specific location. I proposed that the billfish rostrum should have a continuous stress distribution along its length in order to act as a suitable feeding weapon. as this failure that would likely reduce the feeding success of these predators. If species-specific behavior occurs. While this investigation was the first step towards the quantification of the functional role of billfish rostra. the goals of this study are to use FEA to investigate the mechanical performance of different rostral morphologies and to ultimately infer feeding behavior in billfishes from these analyses. Finally.. assuming that each morphology will be suited to better withstand the most common loading regime encounter in nature. Material and methods Two heads. Consequently. Heads were CT scanned with a 64 slice Aquilon Toshiba scanner (Toshiba American Medical Systems Inc.marlin are suited for different feeding repertoires (where blue marlin could withstand multidirectional movement of the rostrum and swordfish seemed more specialized in lateral striking (Chapter 2). Furthermore. a more complete assessment of the mechanical performance of different rostral morphologies is possible at the level of the whole rostrum through FEA. I expect to observe differential patterns of stress and strain energy for each species during different loading regimes.

Rostra were loaded to 200 N in three different planes (lateral. NC. dorso-ventral. allowing for an accurate representation of the changes in material properties throughout its length.568 tetrahedral elements and 141.. This was achieved by the incorporation of a thermal analogy that tightly correlated with the stiffness gradient found in the rostra of billfishes. 2011). Research Triangle Park. representing a feasible point of prey contact during feeding. Completed models were analyzed using a linear static analysis (LSA) in Strand 7 (G_D Computing. and axial) simulating possible striking and spearing directions during feeding. two performance variables were investigated: Von Mises stress and strain energy. USA) with slice thickness ranging from 0. most loadings. Australia) into which material properties and constraints were incorporated. resulting in 597.234 nodes for the swordfish. USA) resulting in watertight models.7 GPa and 4. The former 61 . and constraints (anchoring points) of the models followed experimental parameters from bending tests previously performed on the same specimens (Chapter 2). Minor anatomical corrections and deletion of small artifacts were made in Studio Geomagic (Geomagic. Model constraints were assigned at the base of each rostrum to represent the area of attachment to the head. Inc. Belgium).092 nodes for the blue marlin. Models were meshed using 3-Matics.785 tetrahedral elements and 151.2-15. a thermally-graded model was used to assign stiffness gradients to the tetrahedral elements of the rostrum models (Davis et al.4 GPa in blue marlin and swordfish respectively).2-17. Because the material properties of billfish rostra vary along their length (stiffness increases distally from 6. and loading points were assigned distally at approximately 25 % of bill length from the tip.75-1. The criteria utilized for the construction. Three-dimensional renderings of the rostra (from tip to naris) were performed using Mimics software (Materialise HQ. Sydney. and 623.. CA.Tustin. To aid in our understanding of the form-functional complex of the rostrum.0 mm.

confounding the detection of biologically meaningful maximum stresses (Dumont et al. 55 equidistant points along the rostra were surveyed for stress along a straight line from the loading point to the base at the level of the naris.. 2009). Von Mises stress was standardized by applying a constant ratio of force to area of the rostrum and strain energy was standardized based on constant ratio of force to volume of the rostrum (Dumont et al.. due to tetrahedral elements with high aspect ratios that are needed to capture morphological complexity). 2005).e. Therefore.. 2005). 62 . the rostrum with the lowest strain energy will indicate which morphology may be more likely to withstand that loading regime as less energy is spent in deformation (Dumont et al. 2009). In order to determine if billfish exhibit homogeneity of stress distribution along the length of the rostra.. a correction was performed by removing 2% of the highest stressed elements from the analysis accounting for the 98th percentile of Von Mises stress.. while the latter provides a proxy for energy allocation and deformation of each rostrum. This procedure was not performed for strain energy data since this performance measurement is not sensitive to these computational artifacts (Dumont et al. Artificially high stress values are common in biological FEA models (i. models were standardized to isolate the effects of morphological difference on mechanical performance. Maximum values of VM stress (as opposed to average values) are reported as these more accurately reflect the peak magnitude of the mechanical challenges that the organism has to withstand (Dumont et al. serving as an indicator of whole model efficiency. Model size is a confounding factor when comparing stress magnitudes obtained in FEA. 2009). To avoid these artifacts.variable indicates maximal structural capabilities of the rostra and can reveal the most susceptible area(s) of breakage during a specific loading regime. In this manner. Points were surveyed along the farthest areas from the neutral axes since these areas are the ones under highest stress.

Stress values from the FEA models were compared to those obtained from strain gauges at four equidistant locations along the rostra (Fig. Finally. the loading points were distal and the loads applied were 200 N in lateral and dorso-ventral).1). a linear buckling analysis (LBA) was performed in Strand 7 to obtain a buckling load factor. Because only lateral and dorso-ventral 63 . All applied parameters in the FEA model described in the previous sections (FEA modeling) were also utilized for the validation since they matched the experimental settings (i.For dorsoventral loading. 3. an additional step was necessary to further characterize the mechanical limits of rostrum geometries during axial loading. Consequently. 1976). and for lateral loading these values were taken along the edge of the rostrum. This procedure was repeated three times for each species for both lateral and dorso-ventral loading regimes. and can be used to determine which rostrum will be less likely to withstand axial loading. because axial loadings in long. This procedure was performed only for axial loading and a buckling load factor was calculated for each species. the rostrum was fixed at the base. these values were taken along the outermost dorsal surface. After LSA was performed for all loading regimes. the higher the loading factor the lower the chance of buckling.. This factor is a proxy for the safety factor of the rostrum.e. Model Validation The geometry of the FEA models was validated by comparing predicted VM stresses to experimental stresses obtained from previous bending experiments on the same billfish rostra (Chapter 1). and the linear static analysis (LSA) only estimates bending stress. and stress values averaged. slender structures such as the rostrum may produce buckling instead of bending (Wainwright et al.

VM stress was considerably different among loading regimes with maximum values reaching 62.0. Total strain energy values were also lower in this species. Stress differences equal or lower than 25% between methods were considered acceptable values and a good indicator of the biologically accuracy of the models.5.9.1. lateral and axial loading respectively (Fig. model validations were performed for these two loading regimes.1A). 3. 1.2A-C.6 MPa for dorso-ventral. For example. In swordfish.005 J for dorso-ventral.g. Table 3.3A-C.1. Results FEA models All variables investigated varied between species and among loading regimes. lateral and axial loading respectively (Fig. Only values relevant to each loading regime were compared at each location. during lateral loading only stress from lateral strain gauges (one on each side of the rostrum) were averaged for each region since the stress from dorso-ventral gauges were minor due to their proximity to the neutral axes.7 and 0.1B). 9. Blue marlin VM stresses were lower in all loading regimes. higher stress in the lateral area of the rostrum during lateral loading).2 and 2. 3. reaching 16.1B). lateral and axial loading respectively (Table 3. noticeable differences 64 . Although similar patterns of stress were found in both species for each loading regime (e.0 MPa for dorso-ventral..04 J during dorso-ventral. 19.1A). measuring 3. 1. and 0. lateral and axial loading respectively (Table 3.4. 12. The total strain energy (an indicator of model deformation and mechanical efficiency) was 37.loadings were applied during the bending experiments. Table 3.

2C vs. 3.3A).3C). The lowest stress differences between species were observed during lateral loading where high stress was concentrated on the lateral regions of the rostrum away from the neutral axis (Fig. more proximal areas of the rostrum were also affected in swordfish (Fig.3. Fig. Interspecific differences were greatest during dorso-ventral loading.3. However.4 in blue marlin compared to 1.4). Fig. 65 .2C.in the magnitude of stress were observed between species (visualized in the color coded histogram on each FE model. the application of axial loading resulted in a buckling factor that was approximately ten times larger in blue marlin (12.2. Stress distribution from the 55 points surveyed showed similar values along the rostrum for both species and both loading regimes. Figs. indicating that the blue marlin is less likely to buckle during axial loading. 3. and in most cases differences were considerably less (Table 3.2A vs.3B).1. 3. where larger areas and higher values of stress were pronounced in the swordfish rostrum (Table 3. Model validation Differences in stress between the FEA models and previously estimated experimental values from implanted strain gauges did not differ by more than 25 % for most of the regions. For axial loading both species showed the largest stress in the distal region of the rostrum towards the tip. 3. The differences in stress magnitude between both loading regimes in swordfish were also noticeable. Fig. Blue marlin.5 in swordfish). Stress variations were restricted to the proximal and distal end of the rostrum where stress decreased and this was most noticeable in swordfish during dorso-ventral load (Fig. 3. 3. In addition. D).2B vs.3). Fig. however. 3.2A-D). showed differences higher than expected in area 4 towards the base of the bill for both loading regimes (lateral loading 32% and dorso-ventral loading 39%) (Table 3.

2008). 66 . for example. supporting the hypothesized function for the marlin rostrum (Domenici et al. 2014). B).. total strain energy. documented this species striking prey with a wide range of motions. Moreno et al. 1995. 3. thereby suggesting species-specific feeding behaviors. Stress patterns reported here also agree with those reported from bending experiments for which blue marlin showed similarly low standardized stress in lateral and dorsoventral loading (Chapter 2).1A. In addition. Table 3. low patterns of stress found in blue marlin suggest that this rostrum morphology is better suited not only to withstand higher loads but also to tolerate a broader range of loading regimes.2. the one with lower stress will be more likely to withstand higher loads before failure (Rayfield. a closely related billfish species with similar rostrum morphology.. a recent kinematic study in sailfish. Tables 3. where stress calculated from strain gauges was substantially lower during lateral loading (Chapter 2).3.. 2009).. rostrum morphology appears to be optimized to withstand lateral loading better than other forms because VM stress and total strain energy during lateral loading were the lowest among the three loading regimes (Fig.Discussion The study of logistically difficult systems (e. In swordfish.1A. fast predators like the billfishes) has been facilitated by the application of in silico engineering techniques such as FEA to biological systems. When structures are subjected to the same loading conditions.g. 3. large. Pierce et al. Overall. these FEA results correspond with experimental results for swordfish. 2005. 2004. In addition. Results regarding stress. This was also implied for other long and depressed snouted organisms such as crocodiles (Busbey. B). since VM stress and total strain energy were within similar ranges in both lateral and dorso-ventral loading conditions (Fig. and buckling factor indicate that rostrum morphologies in billfishes are mechanically suited for different functions.

Stayton. Conserved patterns of stress are not uncommon in comparative FEA studies.1A. areas of higher stress were localized along the lateral region of the rostra during lateral loading (Figs 3. suggesting that swordfish are less suited to perform dorso-ventral movements of the rostrum to strike their prey. 3. 3. The rostrum of both billfish species showed a continuous distribution of stress for the majority of the 55 points surveyed along its length. 2004.. corroborating the proposed use of this structure by swordfish. to act as an effective feeding weapon. with the swordfish rostrum exhibiting approximately four times higher stress than blue marlin (Table 3. the magnitude of stress differs among taxa.3B. 2009. 2004).3. suggesting this structure may be optimized for feeding. Fig. the skulls of marmosets and tamarinds and between turtle shells (Pierce et al. as reported in the above-mentioned examples. drag has also been found to be three times greater during dorso-ventral movements than lateral movements of the rostrum in swordfish (Chapter 2).2B. However.3B). 3. Overall patterns of stress along the rostrum were similar between swordfish and blue marlin for each loading regime. However. For example. 2005). Interspecific differences in rostrum stress become more evident during dorso-ventral loading. Strain or stress gradients in bone are not rare. primates and alligators (Ross and Metzger.2A vs. strong gradients of strain have been reported along the skulls of bats. Furthermore. Although similar results were found in a previous study (Chapter 2). contradicting the traditional view about skull optimization for feeding (Ross and Metzger. Fig. 3. 2009.. stress data were gathered from strain gauges in only four locations and since the localized effect of strain 67 . the billfish rostrum has been previously suggested to have a homogenous distribution of stress along its length avoiding any region of high stress concentration that could lead to failure (Chapter 2). 2010). Dumont et al. Results agree with this hypothesis (Fig. Dumont et al. similar patterns of stress were found between the skulls of teleosaurid and metriorhynchid crocodylians.4)..4).

Evidence of this behavior has been reported from prey injuries within stomach contents. or from direct observations (Wisner. perhaps due to their proximity to the loading and anchoring points where stress values were smaller (Fig. van der Elst and Roxburgh. This constant distribution of stress was observed for the majority of the rostrum. thereby buffering the increase in bending moment that otherwise will create a stress gradient commonly reported in other systems. 1981). broken rostra found in prey items. The fact that these differences are more pronounced in swordfish during dorso-ventral loading reflects the differences in changes of cross sectional area towards the base where an abrupt change of geometry is observed. suggests whether this behavior is species-specific as pieces of rostra from different species have been reported embedded in 68 . some differences in stress were observed along the tip and the base of the rostrum. 1984). Spearing behavior has been documented several times for billfish. 1958. however. An abrupt increase in cross sectional area and consequently second moment of area (I) occurs proximally in the billfish rostrum (Chapter 2). including several istiophorid members such as the striped marlin (Tetrapturus audax) (Fig.4).gauges may result in hidden peak stress (Ross and Metzger. 2004). 3. however. 3.5).the current analysis offers a more thorough approach to support this hypothesis. The change in geometry from elliptical to circular favors a decrease in stress during dorso-ventral loading at the base of the rostrum because the neutral axis is positioned further away from the surface of the rostrum. as this compensates for the expected increase in bending moment that occurs with the increase in distance away from the loading point (Currey. Buckling factors suggest that the blue marlin rostrum is 10 times more likely to withstand axial loading than the swordfish rostrum. No previous evidence. A constant stress distribution can be achieved in a cantilever beam by increasing its cross sectional area proximally.

Under both lateral and dorso-ventral loading regimes. in the absence of these parameters. Strait et al. However. Structural integrity is paramount in skeletal elements subjected to continuous loads. especially during dorso-ventral loading. These findings suggest that more energy is allocated for deformation during dorso-ventral loading of the swordfish rostrum. Dumont et al. Whether this is a common feeding behavior in nature remains uncertain. The swordfish’s large strain energy. results suggest that blue marlin. indicating the swordfish rostrum will bend more easily than the blue marlin rostrum under the same load. 2000. Deformation. Although we are not aware of failure parameters for the whole rostrum in billfishes. and facilitating comparisons among species (Dumont et al. Similar conclusions can be reach when analyzing flexural stiffness (EI) values from Chapter 2. 1996).different sources (Frazier et al. Strain energy is a proxy for deformation. 2005. 2009).. reducing its efficiency during prey striking. a variable indicative of overall’s structure resistance to bending. perhaps making this structure less effective than the istiophorid rostrum during this loading regime. may become a critical factor in billfish rostra. areas of highest stress are considered most likely to fail (Keyak and Rossi. the blue marlin rostrum showed lower values of total strain energy. among other istiophorids with similar rostrum morphology. values from three point bending analysis in small bone samples from the rostra of five billfish species may shed some light on the 69 . 1994. for example. 2010). Von Mises stress has been utilized as a proxy for bone failure in FEA when actual failure parameters are lacking. implies that this structure may be subjected to larger deformations under this load than blue marlin. are more likely to engage this type of behavior.. providing useful information for understanding structural performance.. 2009. Flexural stiffness was found to be lower in the swordfish than in the blue marlin rostrum during dorso-ventral loading. Fierstine and Crimment..

Wang. their absence may have resulted in an increase in stress in this region. Poor correspondence between in vivo and FEA models has been attributed to the lack of sutures in FEA models in crocodilians as well (Metzger et al. However. 2003. 2005). white marlin (Tetrapturus albidus). However the most likely explanation may be linked to the lack of sutures in the models. including the proximity of this area to where the model was physically constrained. 2011). 2011). For example. However. 2014).2). area four). While the length of the rostrum is mostly 70 . as constraints have been shown to affect FEA results (Rayfield.understanding of failure parameters. Rayfield 2004. both methods for stress comparisons were performed on the same specimens. Considering white marlin is the closest relative billfish species with known failure parameters (Santini and Sorenson. 400 N) to result in failure of the swordfish rostrum during dorso-ventral loading.1. Rayfield 2005. 2007). since sutures were not replicated in the FEA models. particularly at the most proximal region of the rostrum (Fig. especially in blue marlin (Table 3.. increasing certainty in the results (Panagiotopoulou et al. Several factors may account for these results. some variation between the experimental and modeled stresses was observed. In addition. where values of stress from FEA were substantially larger. Stress differences from the validation analysis were for the most part less than 25% different from the experimental stress suggesting the models fell within an acceptable level of biological accuracy. have been reported to fail at approximately 120 MPa (Atkins et al. since sutures have been shown to be stress/strain dissipaters and shock absorbers in the vertebrate skull (Rafferty.. if material properties are considered to be conserved in this group and accounting for a linear model of elasticity. Owing to its proximity to the skull.. 3. multiple sutures are present in area four. An alternative explanation for these results may be linked to the proximal increase in complexity of the rostrum. 2013). it would take at least two times greater load than the one applied in this study (approx.

comprised of acellular bone. 2013). a recent study found no implication in drag reduction when modeling different rostrum lengths in two billfish species (Sagong et al. A recent theoretical approach. 2005). however. Swordfish. 2013). Although the rostrum in billfishes is mechanically suited to function as a feeding weapon... 2011.. proposed that hydrodynamics may play a role during feeding. 2012). where blue marlin may strike its prey with a wider range of motions 71 . Species-specific feeding behaviors seem to be morphologically dependent. These materials were not including in the models. the composite nature of bird beaks facilitates seed crushing in Darwin’s finches by increasing their stiffness to weight ratio (Soons et al. and ignoring the composite nature of biological structures has been suggested to impact FEA models (Rayfield. A hydrodynamic role has been hypothesized. and increases energy absorption in the toucan beak (Seki et al. for example. regardless of its morphology in swordfish and blue marlin. Composite materials are common in nature as they exhibit emergent properties not possible for individual materials. For example. other biological roles may be important in its evolution. In conclusion. the base is filled with adipose tissue and hyaline cartilage (Chapter 1). were shown to be specialized for lateral movements of the rostrum (as suggested in the current study) since values of stress and drag were the lowest during this loading regime while applying a continuous load along the rostrum. Meyers et al. simulating the effect of feeding in water (Chapter 1). however. as was suggested for the cancellous bone in the ostrich mandible or other foam like core fillings in nature (Rayfield. These materials have been proposed as stress/strain dampeners or shock absorbers in billfish (Gudger. evidence indicates that the billfish rostrum is mechanically suited to act as a feeding weapon owing to the homogenous distribution of stress along its length. 1940).. 2011).

E. Kitchener. R. Withers. commonly cited examples of “swordfish” piercing wooden ships. C. P.org/10.1098/rsif.L....org/10. Steffensen. Proc. M. J. Brassey. J. Couillaud.D. Currey. A.A.. A. P.doi. 319-330. Grosse I. Y.L. O.. Biol. M. NJ: Princeton University Press. Interface 10: 20120823. P. Dean.M. Sellers. Habegger. Herbert-Read.E. Rec. S.M.. and Shahar. (2009) Requirements for comparing the performance of finite element models of biological structures. Atkins. P. (2005) Finite-element analysis of biting behavior and bone stress in the facial skeletons of bats. 96-103.J. Domenici. R. (1996).. Kurvers. 283.than swordfish. Wilson. S.J.G. J. Soc.2014. and Krause. 1996. S.. (2012). W.. dx.D. Dumont E. P. Soc. However. Grosse I. Finite element modeling versus classic beam theory: comparing methods for stress estimation in a morphologically diverse sample of vertebrate long bones. Piccirillo J. How sailfish use their bills to capture schooling prey. Motta...J. Theor. A. (1977). the latter being better suited for lateral striking. The Hague. 256.. Marras. Whether the rostrum of either species has evolved to accomplish these feeding roles remains uncertain. doi/10.J.1412372111. Princeton. Krause. Junk.. E. (2014).. References Aleyev.I.0444..0823. Manning.R.C.doi. J. Roy. (1984). J. The Mechanical Adaptations of Bone. and Crimmen.. Currey. R. http://dx.1073/pnas..R. Slater G. Fierstine. Margetts. Remodeling of anosteocytic bone.R.1098/rspb.. 72 . Nekton. results from this study support feeding as the primary function of the rostrum in billfishes.2012.L.. Two erroneous. (2014). Copeia.R. Viblanc. 472-475.H.. Anat. P. H. PNAS. Dumont. J. L.

Chelonia: Cheloniidae and Dermochelyidae) by billfishes (Osteichthyes.R. Env. Mackie). Isurus oxyrinchus. 117-121.209-214.. 73 . S. McHenry. Yamaguchi. (1997). Cailliet. and Prigioni. E. Biomech. and Pendharkar. Fish. The biomechanics of the rostrum in crocodilians: a comparative analysis using finite element modeling. H. M. Soc. Zool. 33. McGowan. C. C. S. In: Coelenterate Ecology and Behavior (ed. The allegated pugnacity of the swordfish and the spearfishes as shown by their attacks on vessels.. H. (1994). 39.G. Mem. Prediction of femoral fracture load using finite element models: an examination of stress. Fierstine. 85-96. J. A. Shortfin Mako. Rec. and Neer. W. Keyak. Clausen. F. impaled by two species of billfishes (Teleostei: Istiophoridae). J.. 496-503.W. M. 3. Asiatic. Makaira nigricans (Teleostei: Istiophoridae). S.A...A..A (2000). (1976). 2. Impalement of marine turtles (Reptilia.L.L. 66. G.O. Perciformes: Istiophoridae and Xiphiidae). Calif. Koehl. Hiroyuki. South. Gudger. J.Frazier.J. 495-499. Roy. Acad. 61. (1997). Fierstine. P.M. Fierstine. 827-849. G.R.L. Plenum Publishing Corp.. (1940). Y. Can. impaled by blue marlin. An Atlantic Blue Marlin.B. Mar. J.M. Bull. Beavers. Daniel. Biol.. Sci. Anat. Pitman.T. Sci. Achaval. H. (2006). 288. and Rossi. R.H.C. 215-31. J.. (1988). Meers..L. Differential development of the rostrum and mandible of the swordfish (Xiphias gladius) during ontogeny and its possible functional significance. Makaira nigricans. Mechanical Design in Sea Anemones.and strain-based failure theories. C. Bengal Branch. Bull.

35. S. 257-233. Strain in the ostrich mandible during simulated pecking and validation of specimen-specific finite element models. No. (2003). J. 283. 212. Using finite element analysis to investigate suture morphology: a case study using large. Ecology and functional morphology. McHenry.D. E. S. 255-396.. Anat. Rec.J. K. Lab.0081323. carnivorous dinosaurs. Seto Mar. Jeon. (2004). Rayfield. Nakamura.J. Earth Planet Sci. FAO Species Catalogue.J. E. K. E. Anat. Wroe. Rayfield. 271. B. (2008). E.W and Marshall. 349-365.. Isr. V. J.pone.Moreno. C. W. FAO Fish.. Swordfish and billfishes in the Atlantic Ocean. 74 . Cranial performance in the Komodo dragon (Varanus komodoensis) as revealed by high resolution 3-D finite element analysis. Lond. Rev. Systematics of the billfishes (Xiphiidae and Istiophoridae). Billfishes of the world. Herring. Publ.. I. P. Cunningham. Morph. Prog. Biomechanics of the rostrum and the role of facial sutures. C. J. E. (2007) Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. 1-65... I.P.C. 47-58.. (2005). Proc. (1985). (1983). Annu. 736–746. Royal Soc.. PLoS ONE doi:10. Anat. Synop.L. Rayfield. Trans. Sagong. Hydrodynamic characteristics of the sailfish (Istiophorus platypterus) and swordfish (Xiphias gladius) in gliding postures at their cruise speeds. (2011). 541-576. Sci. D’Amore. 1451-1459. Choi. Rayfield. 28.V. Nakamura. Ovchinnikov. E. (2013). Rafferty. Clausen. (1970). Rayfield. Cranial mechanics and feeding in Tyrannosaurus rex. 213. D. H. W.125 5. 44. Biol. NOAA NMFS TT 71-50011.1371/journal.J.

Ross. C. M. (1964). Surface strain on bone and sutures in a monkey facial skeleton: an in vitro 75 . Princeton University Press. E. Biol. K. Fish. Bd. Wright. in the Western North Atlantic. (2007). C.A. J. and Penrih. Linn. and Meyers M. B. 51-67. B.S. Ichtyol. Byron. T.B.D. Pol. Istioampax marlina. Food and feeding ecology of the swordfish Xiphias gladius in the western North Atlantic Ocean with estimates of daily ration. Canada. (1976). K. 51. S. J.P. Res.A. NJ. (2006). Currey. Spence. and Roxburgh. Use of the bill during feeding in the black marlin (Makaira indica). and Kohler. 96.. (2009). 25. 22. and Tachihara. D. 468.. 239-247.. 215. Tseng. Henderson. Cranial function in a late Miocene Dinocrocuta gigantea (Mammalia: Carnivora) revealed by comparative finite element analysis..S. Copeia 1964.Seki. Strait. Princeton.J.N. J. Wainwright. J. Snively.. Wang. Saito.M. D.E.S. 435-454.. Fused and vaulted nasals of tyrannosaurid dinosaurs: Implications for cranial strength and feeding mechanics. (1985).M. Soc. Ecol. C. Structure and mechanical properties of the toucan beak. 903-972. 53. Shimose. (2005). Q. 54.. Stillwell. Mar. J.. Spearing behavior in feeding in the black marlin.. M. Food and feeding habits of swordfish. 5281-5296..C.A. Richmond. P. Scott.D. Evidence for the use of the bill by blue marlin (Makaira nigricans). Dechow. Yokawa. Res. Z. M. (2007). and Phillips. W.. W. Van Der Elst.E. during feeding. D.. (1968).H. R. and Gosline. Y.J. Acta Paleon. Xiphias gladius. Schneider. 420-422. Mechanical Design in Organisms. (1981).D.F. Talbot. Acta Mat.. M.. and Tibbo. S.W. F. Biggs. N.G. Copeia 1981.

Wisner. CEWall. In Primate Craniofacial Function and Biology. 12. (1958). Sci. 76 . MJ Ravosa. New York: Springer. R.method and its relevance to finite element analysis. Is the spear of istiophorid fishes used in feeding? Pac. ed. CJ Vinyard. 60-70.

1. lateral and axial) in two billfish species. B) Strain energy (J) Swordfish Blue marlin Dorso-ventral 37. gladius) and blue marlin (M.04 0. the swordfish (X. gladius) and blue marlin (M.67 1.01 *Total strain energy for three loading regimes (dorso-ventral.5 16.1 Lateral 19.45 Axial 0.0 *Maximum values of von Mises stress for three loading regimes (dorso-ventral.09 Lateral 9. The swordfish (X. Stress values (A) and total strain energy (B) in two billfish species.6 1. A) von Mises stress (MPa) Swordfish Blue marlin Dorso-ventral 62. the swordfish (X.2 12. nigricans) 77 . lateral and axial) in two billfish species. gladius) and the blue marlin (M.Table 3.93 3. nigricans) during three loading regimes.0 Axial 2. nigricans).

5 ± 0.5 AREA 3 10.8 31.4 ± 0.2 15.8 ± 1.3 AREA 4 5.6 ± 0.4 14.1 ± 0.0 ± 0.0 8.5 14. 78 .9 BLUE MARLIN (dorso-ventral loading) MTS FEA % DIFF AREA 1 10.4 13.1 7.0 ± 0.8 AREA 3 2.5 ± 0.2 38.2 AREA 2 2. SWORDFISH (lateral loading) MTS FEA % DIFF AREA 1 1.2 ± 0.0 2. Bold print indicates value greater than 25% different.5 9.0 10.4 AREA 4 5.0 2.4 ± 0.7 ± 0.7 SWORDFISH (dorso-ventral loading) MTS FEA % DIFF AREA 1 2.0 AREA 3 2.0 2.4 12.7 ± 0.8 ± 0.3 ± 0.6 ± 0.8 Stress values (X±SE) were compared for four areas along the rostrum of two billfish species the swordfish (X. nigricans).2 13.0 AREA 2 13.1 18.7 ± 0.8 ± 0.0 BLUE MARLIN (lateral loading) MTS FEA % DIFF AREA 1 10.0 ± 0.7 AREA 2 2.0 7.3 ± 0.8 ± 0.Table 3.1 2. Differences between both methods are indicated by % DIFF for each area and each loading regime.8 16.8 AREA 3 13.1 ± 0.1 5.7 ± 0.3 12. gladius) and the blue marlin (M.7 ± 0.6 ± 0.1 14.2 12.7 AREA 4 2.6 ± 0.4 ± 0.2 3.2 AREA 4 1.1 13.4 ± 0.1 2.0 2.4 ± 0.7 ± 0.0 2.2.1 ± 0.2 ± 0.1 17. Experimental and predicted stress means (MPa) compared for FE model validation.6 25.6 AREA 2 12.1 7.2 14.1 ± 0.

Outline of the experimental settings and the FEA results of a swordfish rostrum (X gladius) during lateral loading showing the areas of stress used to validate FEA model’s geometries. Strain gauges (SG) were attached along the rostrum in four areas (1-4. Top diagram outline of a swordfish rostrum used during bending experiments in a material testing system (MTS). 3. Note that the colors on the FEA diagram are only for illustration purposes no quantitative data is shown 79 . Values of stress from FEA indicated with an “x”.1. were obtained from the same position where SG.Fig. distal to proximal) and load was applied distally at the loading point (LP).

were cool colors denote low stress and warm colors denote high stress. B) lateral and C) axial loading. Red arrows indicate loading points as well as the direction of loading.Fig. gladius) for three loading regimes A) dorso-ventral. The isolated rostrum used for FEA is delimited between dashed lines. Predicted von Mises stress distribution in the swordfish rostrum (X. The blue areas at the two most extreme point of the rostrum: distal (tip of the rostrum) and proximal (base of the rostrum) are the loading points and anchoring points where not stress was quantified. In some cases (dorso-ventral loading) colors exceeded the upper limit of the histogram indicating even higher stress. Three dimensional renderings of whole skulls are shown in lateral view (top left) and dorsal view (to right). 80 . 3. Color coded histograms associated to each loading regime indicates the relative amount of elements on each stress state.2.

Color coded histograms associated to each loading regime indicates the relative amount of elements on each stress state. Three dimensional renderings of whole skulls are shown in lateral view (top left) and dorsal view (to right). 3. nigricans) for three loading regimes A) dorso-ventral. Predicted von Mises stress distribution in the blue marlin rostrum (M. The blue areas at the two most extreme point of the rostrum: distal (tip of the rostrum) and proximal (base of the rostrum) are the loading points and anchoring points where not stress was quantified.Fig. B) lateral and C) axial loading. Red arrows indicate loading points as well as the direction of loading. 81 . The isolated rostrum used for FEA is delimited between dashed lines. were cool colors denote low stress and warm colors denote high stress.3. In some cases (dorso-ventral loading) colors exceeded the upper limit of the histogram indicating even higher stress.

gladius) (left) and blue marlin (M. Full blue regions beyond this point are outside the range of any stress. 3.Fig.4. Dashed arrows indicate the limits where samples were taken. starting point (0 rostrum length) and the end point close to the loading point (55 rostrum length). Stress distribution (mean±SE) along 55 points of the rostrum in swordfish (X. nigricans) (right) during lateral loading (black dots) and dorso-ventral loading (white dots). 82 .

Photograph taken by Doug Perrine. audax). a closely related species to blue marlin with similar rostrum morphology. 3. 83 . Although it is not known whether this is a common feeding behavior. occasional spearing events have been documented for blue marlin (Frazier et al.Fig. Spearing event in a striped marlin (K. 1994).5..

It is expected that apex predators rely in high biting performance to occupy higher trophic positions. because an increase in bite force may allow access to mechanically challenging prey or result in increased dietary breadth. In addition. Billfish are apex marine predators characterized by an extreme elongation of the upper jaw bones forming a rostrum. but little is known as to whether this modified structure has resulted in a decrease in biting performance due to the concomitant release of selective pressure on the jaws for prey capture. This structure has been shown to facilitate prey capture and processing. Because prey processing is in this case partially decoupled from the oral jaw. and the relationship of bite force to cranial anatomy including rostrum length. due to their large size and the concomitant increase of the adductor muscles size. Consequently. the goal of this study is to investigate bite force in five billfish species differing in size and rostrum morphology. with greater reliance on rostrum length and hence 84 . we expect intraspecific variation in mass specific bite force to be predicted by rostrum length. CHAPTER FOUR FEEDING BIOMECHANICS AND THEORETICAL CALCUALTIONS OF BITE FORCE IN BILLFISHES Abstract Bite force is one of the most utilized performance measures due to its relationship to feeding and consequently fitness. we hypothesize that bite force may be relatively low in billfishes compared to other fishes.

. 2012). Results indicated that anterior values of bite force ranged from 29 to 330 N in billfishes and posterior values ranged from 99 to 1361 N. Herrel and Holanova. 2006). has been demonstrated to have a role in feeding. because harder 85 . indicating that the rostrum may augment these biological roles. (Archorsagus probatocephalus.. intraspecific combat (Husak et al. to be inversely proportional to bite force. 2008).. The investigation of bite force has significantly contributed to our overall understanding of organismal ecology as it is not only linked to feeding ecology.processing.. Kolmann and Huber. Bite force may be related to dietary specialization with high bite force found in durophagous species such as chameleon lizards (Chamaeleolis. Herndandez and Motta. mass specific bite force was amongst the lowest compared to other cartilaginous and bony fishes. however. 1997). 2010). and horn sharks (Heterodontus francisci. 2006) as well as burrowing efficiency in vertebrates (Van Daele et al.. Even though absolute bite forces were high in some species. but is also related to mating success (Lappin and Husak. 2001. The evolution of this novel structure. Introduction Bite force is a broadly utilized metric of feeding performance because of its perceived association with fitness (Binder and Van Valkenburgh. 2008). Herrel et al. allowing the exploitation of differing dietary niches (Dumont et al. and the relatively low bite force in billfishes may indicate a lack of dependence on this performance metric for prey capture and processing. Huber et al. 2000. Contrary to my second hypothesis. bony fishes such as the sheepshead. 2005). High bite forces have been shown to affect prey processing (reduction of prey to edible size). facilitating their feeding success as apex predators. rostrum length was not a predictor of bite force.

biters can reduce the amount of time utilized to subdue and reduce prey, perhaps increasing

energy intake as shown in lizards (Verwaijen et al., 2002).

Prey capture methods can also influence bite force, in fact, it has been long assumed that

suction feeding and biting performance may be under conflicting demands (Barel, 1983), as the

mechanism of force transmission may limit the speed at which jaws can be closed (Herrel et al.,

2002). As a result predators that rely in fast jaw closure to capture evasive prey may not produce

large bite forces (De Schepper et al., 2008).

Biting performance has a strict association to size within and among species; a common

pattern found during growth is a disproportional increase in bite force owing to rapid increase in

head or muscle size (Herrel and Gibb, 2005, Herrel et al., 2005). It is expected that size alone

will be responsible for large bite forces as seen in sharks or alligators (Erickson et al., 2003, 2012

Huber et al., 2006). Alternatively, some large predators have disproportionally low biting

performances for their size, as complementary feeding structures may replace the need for high

bite force. In the Komodo dragon (Varanus komodoensis) for example, bite forces have been

shown to be relatively weak and it is suggested that venom glands are in part responsible for

their predatory success, not high bite force per se (Fry et al., 2009).

Changes in dentition may also help to overcome bite force limitations (Herrel et al.,

2004). Shark teeth and fast strikes by some bony fishes including king mackerel

(Scomberomorus cavalla) and great barracuda (Sphyraena barracuda) may override the

necessity for high bite force as these apex predators have amongst the lowest mass specific bite

forces of fishes (Habegger et al., 2010, Ferguson, 2014). In addition, biting species that feed on

fast elusive prey may sacrifice powerful jaws for speed efficient ones such as the gharial with its

long, narrow rostrum (Gavialis gangeticus, Gavialidae) (Erickson et al., 2012).

86

Billfishes are fast pelagic fishes that are characterized by an extreme elongation of the

upper jaw into a bill or rostrum. The rostrum differs in relative length and morphology; for

example, the swordfish (Xiphias gladius) rostrum may attain lengths up to 50 % of its body

length, its cross section is lenticular and lacks teeth along its length. In shortbill spearfish

(Tetrapturus angustrirostris), the rostrum may only exceed lower jaw length by a few

centimeters, and its cross section is oval to round and has small villiform teeth (Nakamura,

1983). The function of the rostrum is controversial (Nakamura, 1983, Frazier et al., 1994). It has

been suggested to play a role in defense, to increase hydrodynamic efficiency, or to aid in

feeding (Wisner, 1958, Ovchinnikov, 1970; Aleyev, 1977). The latter has been based in part on

examination of stomach contents of some istiophorids such as blue marlin (Makaria nigricans),

which show evidence of prey cut in half, punctured and lacerated (Shimose et al., 2007, 2008).

Acting as a spear in most billfish species, this structure is able to injure, immobilize or even kill

prey before ingestion, facilitating prey processing and capture (Gudger, 1940; Talbot and

Penrith, 1964, Scott and Tibbo, 1968). In addition, recent biomechanical testing in several

billfish species and kinematic studies of Atlantic sailfish (Istiophorus albicans) has supported

feeding as the most plausible role (Atkins et al., 2014, Domenici et al., 2014).

The goal of this study is to investigate bite force and its relationship to rostrum length in

five billfish species exhibiting different rostrum morphologies. Given that the billfish rostrum

may allow for pre-processing of prey before ingestion, it is hypothesized that this attribute might

reduce the selective pressure for high bite force. Therefore, billfish should have relatively lower

bite force compared to other fishes. Furthermore, we expect interspecific variation in bite force

to be inversely proportional to bite force as prey processing is partially decoupled from oral jaw

processing in billfishes.

87

Material and methods

A total of 33 specimens (five billfishes species and one scombroid species) were

collected from recreational fishing tournaments and commercial fisheries along the Gulf of

Mexico, the Florida Keys, Ocean city, Maryland and Hawaii and kept frozen until dissections

were performed. The billfish species were selected to represent a wide range of rostrum

morphologies and taxa according to the latest phylogeny (Santini and Sorenson, 2013). Species

collected include blue marlin (Makaira nigricans, N=6), swordfish (Xiphias gladius, N=6), white

marlin (Tetrapturus albidus N=6), shortbill spearfish (Tetrapturus angustrirostris N=5) and

sailfish (Istiophorus albicans N=3). In addition a non-billfish species, the wahoo

(Acanthocybium solandri) was collected (N=6) and assigned as the outgroup for comparative

purposes (Santini and Sorenson, 2013). Variables including body mass and rostrum length (from

tip to orbit) were taken when possible (Table 4.1). In cases when data were not available,

extrapolations were performed from meristic regressions made from known datasets and

photographs (sailfish: Prager et al., 1995; shortbill: Silkman and Yong, 1974, wahoo:

Breerkircher, 2005).

Anatomical descriptions

The anatomy of the jaw adductor muscles were described. Dissections were performed on

the left cheek of each specimen and identification of the adductor mandibulae complex was made

following Winterbottom (1974), Davie (1990), and Fierstine (Pers. comm.).

88

As all muscles were parallel fibered. and the most proximal margin of the teeth was designated as the posterior bite force point (PBF). anatomical cross sectional area (CSA. the A1+A2 subdivisions were dissected as one. The most distal point of the lower jaw was designated as the anterior bite force point (ABF). USA) using Sigma Scan Pro version 4 (SYSTAT Software Inc. mm2) were traced from digital photos (Canon Power Shot A710is. Theoretical maximum tetanic force (Po) for each subdivision was determined by multiplying the CSA by the specific tension of fish muscle (TS) (20 N/cm2. perpendicular to the main fiber direction. or the distance from the jaw joint to each muscle insertion and out-lever (OL). USA). 1982) following Powell et al.Theoretical calculations of bite force The major subdivisions of the adductor mandibulae were removed and bisected through their center of mass. USA). jaw joint. Altringham & Johnston.. Polhemus. Canon Inc. (1984). Po = CSA x TS After the muscles were dissected from the skulls. 89 . Swordfish teeth were not visible. Colchester. the jaws were adducted and three-dimensional coordinates of origin and insertion of each adductor subdivision. NY. as most comparative studies of bite force in fishes do not consider the contribution of Aw due to its size and location. or distances from jaw joint to each bite point were measured. VT.. this subdivision was not incorporated in the current analysis. therefore the posterior bite force point was traced by hand and located when the ridged surface of the jaw terminated. In-lever (IL). Furthermore. CA. Because the two most superficial subdivisions were difficult to isolate. Point Richmond. and two bite points along the lower jaw were gathered for each individual of each species using a three dimensional digitizer (PATRIOTTM digitizer..

(2005): FLJ= FJR+FAM1+2+FAM3+FB = 0 Where. all data were size-corrected by weight using the phylogenetically-corrected method outlined by Revell (2009) and implemented in the R package phyTools (Revell. and because animal mass is related to bite force. Since the traits from each species do not represent phylogenetically-independent information in a regression framework (Felsestein. FAM3 were forces generated by each adductive muscle subdivision and FB was bite reaction force from the prey item. USA). 2012). MA. A full Brownian motion model of evolution was 90 . Size- corrected trait values were then analyzed with both ordinary least squares (OLS) and phylogenetic generalized least squares (PGLS) regressions assuming trait evolution via Brownian motion (Grafen. FLJ were forces acting on the lower jaw.Mechanical advantage (MA) was then calculated as the ratio between the in lever and the out lever. FJR were jaw joint reaction force. FAM1+2. following Huber et al. 1989. 2010). Cambridge.. The theoretical tetanic force and 3D position for each muscle were used to calculate three dimensional force vectors produced for each adductor mandibulae subdivision. Theoretical maximum bite forces produced along the lower jaw were calculated via summation of moments about the jaw joint with a 3D static equilibrium model in Mathcad 13 (Mathsoft. 1985). Inc. 2001). Rohlf.. Bite force predictors All data were log-transformed to account for some skewness in trait measurements (Zar.

1).. 2007) assuming a maximum likelihood estimator (ML). 37 candidate models were compared. and PGLS had an additional Brownian correlation structure defined by the corBrownian() function from the ape R package (Paradis et al. cross sectional area of the subdivision of the adductor muscles (A1+A2).. We first aimed to identify the importance of each variable in predicting bite force by estimating their relative importance using the summed AICc weight of all models in which predictors appear (Buckland et al. 4. The phylogenetic tree used in size-corrections and phylogenetic analyses had a topology based on Santini and Sorenson (2013) and internode divergence times based on Santini and Sorenson (2013) and Hedges et al. We limited the complexity of these candidate models to up to two simultaneous predictors (and intercept) to avoid regression over-fitting relative to the small sample size (Zar. and cross sectional area of the subdivision of the adductor muscles (A3). Model comparisons were based on Akaike’s information criterion corrected for small-sample bias (AICc. This procedure generates regression models by assigning a weight to every predictor. 2004).assumed for all PGLS analyses because there were too few species (N = 6) to confidently estimate lambda-fitted (phylogenetic signal) models (Lajeunesse. since they are normalized their sum equals one (Marshall 91 . 2010). 2008). To identify the best predictors of bite force. In press). (2006) (see Fig. posterior out lever (POL). and were estimated for all OLS and PGLS candidate models using the glmulti R package (Calcagno & Mazancourt 2010). in lever (IL). we compared all candidate OLS and PGLS models fitted with combinations of main effects without interactions using up to two predictors of bite force. anterior mechanical advantage (AMA).. Both the OLS and PGLS analyses were fitted using the gls() function from the nlme package (Pinheiro et al. anterior out lever (AOL). In total. posterior mechanical advantage (PMA). these models were constructed using the following pool of predictors: bill length (BL). Anderson. 1997).

whereas the position of the most posterior teeth varies greatly. but also present all models that provided considerably less support based on delta AICc < 7. These raw and phylogenetically-corrected residual values were compared and ranked among all billfish species and the wahoo (outgroup).. 2001. 2006. Because all billfishes share a common ancestry. 2010).. For the comparison of bite force among billfishes and other non-billfish species. only ABF is considered further because this position is anatomically determined by the anterior margin of the mandible. 2002). 2004. 1985). we then determined the top candidate models to those fitting a substantial support criteria of delta AICc < 2. and OLS and PGLS regressions were performed with the average for each species against body mass to obtain size-removed bite force residuals. Failure to account for phylogeny during data correction such as size removal can lead to spurious results among tip taxa (Revell. 2010). Following Burnham and Anderson (2002). 2005. In addition ABF is most commonly used for comparative purposes in fishes (Korff and Wainwright. Huber et al. Bite force within billfishes Raw values of anterior bite force were log transformed. each individual data point is not independent (Felsestein. and reptiles (Herrel et al...8 provide strong predictive support (Calcagno and Mazancourt. 1999. 2005). therefore size-removed bite force was corrected for phylogeny following the methods outlined in the previous section.et al. Habegger et al. 2009). Values of relative importance near and above 0. mammals (Wroe et al.0. 2012). perhaps because this bite point position is easier to measure in the field. 92 .0.

2005). bull shark (Carcharhinus leucas. Habegger et al. OLS regressions were used. bite forces from durophagous fish were excluded from the analysis). the great barracuda (Sphyraena barracuda. 2006). The point of insertion between A1+A2 is not clearly defined. Anterior values of bite force were gathered for the blacktip shark (Carcharhinus limbatus. which in turn fills the Meckelian fossa of the lower jaw. The most superficial area of the cheek is occupied by A1+A2.. This subdivision originates along the suspensorium (hyomandibula. 2012) and kingfish mackerel (Scomberomerus cavalla. Only species with similar feeding ecology or diet were included (i. 2010). most of the connection is made by a sheath of connective tissue that expands from the maxillomandibular ligament enveloping Aw. Mass specific anterior bite force was obtained from residuals and compared among species. Separation of A1 and A2 was not possible and they were therefore considered as one. Huber. Huber et al. the largest subdivision. 2014). preoperculum.. A3 and Aw). Results Anatomy The adductor mandibulae complex in billfishes and wahoo is comprised by four subdivisions (A1+A2. lemon shark (Negaprion brevirostris. Since this insertion is broad 93 . Ferguson. metapterygoid). phylogenetic corrections were not applied. attaches partially to the maxilla. Because of the broad phylogenetic range of these species.Bite force among fishes To assess how billfish bite force ranked among other fish species (bony fish and elasmobranchs).e.. with the majority inserting on Aw. Habegger et al.

for the purpose of bite force calculations the insertion point was determined as the center of mass of Aw.57 ± 0. mean ±SD).54 ± 0.3 cm (wahoo and blue marlin respectively).1). The anatomy of the adductor mandibulae.5 N). Anterior mechanical advantage ranged from 0. Anterior out-lever varied from 18. insertion and patterns of muscles size seemed mostly conserved among all species examined (Fig.3. In-lever lengths varied from 4.0 N (wahoo and blue marlin respectively).33 ± 0.83±48.15 (wahoo and white marlin respectively). Shortbill spearfish had the lowest anterior bite force among istiophorids (37.06 to 1. Table 4.53 N) and swordfish and sailfish had the most similar values among billfishes. Posterior bite force values ranged from 98.97 ± 38. Bite force and biomechanical parameters Anterior values of bite force ranged from 29.96 cm (shortbill and blue marlin respectively).29 cm and posterior out- lever ranged from 4.62 ±3. although shortbill spearfish still had the lowest absolute bite force within istiophorids.38 ± 1.and not specific.16 to 329.48 to 10.02 to 0.27. 4.6 N (wahoo and blue marlin respectively. swordfish now had the lowest values among billfishes (158.97 ± 40.24 ± 0. including general origin.1 ± 2. Posterior mechanical advantage ranged from 0.03 to 38.18 ± 10. All istiophorids had values above 1 and swordfish 94 .2 and 4.0 (swordfish and blue marlin respectively).45 ± 0.67 ± 0.46 to 10 ± 0. Shortbill spearfish and white marlin had the same values (0.32 to 1361 ± 184.26) as well as sailfish and blue marlin that had 0.27 ± 0. The deepest subdivision A3 originates mostly on the hyomandibula but also on the preopercle and metapterigoid and inserts by a tendonous insertion on the sesamoid bone of the articular.

The high AICc ranking of the intercept-only model (i.85 (shortbill and blue marlin respectively).2). the most basic model that can be fitted to the data) indicates that none of the predictors (with the exception of CSA of A1+A2) were helpful in explaining variation in anterior bite force.1.66 ± 0. Muscle cross sectional area was larger for the most superficial subdivision (A1+A2) in all species. All results are also summarized in Table 4.13 ± 3. For all compared regression models. intercept-only model. the intercept-only model). Bite force predictors Based on the model selection criteria using AICc scores (Akaike’s information criterion corrected for small-sample bias.).e.57 ± 0. Similar results were observed for posterior bite force (PBF) for the non.68). and again a model with no predictors (i. only the regression model that included CSA of A1+A2 emerged as the best fit (Table 4. with PGLS regressions three models emerged as having strong predictive power of PBF: a model with only CSA of A1+A2.e. see Table 4.phylogenetically corrected (OLS) regressions.93 ± 0. rostrum length (BL) was not a predictor of bite force in billfishes. and ranged from 2.e. When phylogenetic relationships were taken into account using PGLS. similar to that of wahoo (0. two OLS regression models emerged as having equally good predictive power of anterior bite force (ABF): a model with CSA of A1+A2 as a predictor and a model that contained no predictors (i. a second with only anterior out- lever (AOL). 95 .92 cm2 (wahoo and blue marlin respectively) and for A3 from 1.2).24 to 9.was the only billfish to have values below 1.92 to 29. however.

Bite force among fishes Compared to other fishes species with similar feeding ecology or diet. the mass specific bite forces of billfishes are relatively small (Table 4. Sharks typically ranked the highest.1).4).62 ± 96 . this rank remained the same when residuals where phylogenetically corrected (Table 4.Bite force within billfishes Absolute values of ABF were highest for blue marlin and lowest for wahoo (Table 4. some non-billfish species including the wahoo and king mackerel were often nested among the billfishes. with the bull shark showing the largest value of relative bite force.4).6 N. Bite force in billfishes Absolute values of ABF ranged widely in billfishes. 4. mean ± SD) and shortbill spearfish the lowest bite forces (ABF=37. bite force may not be the central contributor to predatory success in some lineages. Although billfish typically occupied the lowest ranks.3. with blue marlin showing the highest (ABF: 329. Discussion As a proxy of performance.4). When size was taken into account size specific anterior bite force was largest for white marlin and lowest for sailfish. however the blue marlin had the lowest mass specific bite force of all species (Table 4. Fig. bite force allows us to understand the maximum capabilities that a predator may need to overcome the mechanical challenges imposed by prey. as shown in this study. However.97 ± 40.

3.53 N). Because larger animals will bite harder owing to an increase of their muscle CSA

(Herrel et al., 2005), this variation is intuitive by virtue of the large range in sizes of the species

examined (15-219 kg respectively). Considering absolute bite forces as a measure of predator’s

maximal performance blue and white marlin stand out among billfishes.

When comparing anterior bite force among species, rankings can vary substantially with

regards to relative or absolute values; as seen in other studies where small, often durophagous,

species are compared (Huber et al., 2008; Grubich et al., 2012). In billfish, however, the rankings

of absolute versus relative bite force did not differ greatly (Table 4.3 and Fig. 4.4). Relative bite

forces were largest in the white and blue marlin; whereas swordfish, sailfish and shortbill

spearfish showed the smallest values. Furthermore, phylogenetic-corrections did not change

these rankings; suggesting these patterns of bite force are not due to phylogenetic relatedness.

However, recognizing the small number of species compared (N=6), phylogenetic conclusions

should be taken with caution.

Bite force predictors

Bite force predictors provide a window into the determinants of biting performance.

Measurements of cranial morphology such as head length, head width, and head depth have been

shown to be good proxies for biting performance in some fishes (Carothers, 1984; Wainwright

1987; Huber et al., 2006, Habegger et al., 2012) facilitating rapid estimations of organismal

performance.

Contrary to my hypothesis, rostrum length (BL) was not a good predictor of biting

performance among billfishes. Although the shortbill spearfish (the species with the shortest

97

rostrum) had one of the lowest relative values of relative bite force, swordfish (the species with

the largest rostrum) also had low values, partially fulfilling one of my hypotheses.

Although rostrum length was not a predictor of bite force within billfishes, several other

predictors were explored. Of all the tested predictors, A1+A2 CSA repeatedly emerged in both

OLS and PGLS regressions as having strong predicative power of bite force (see Table 4.2).

Based in the anatomical descriptions, these results are intuitive since A1+A2 adductor

subdivision was consistently the larger CSA, whereas A3, was the smallest and most variable

subdivision in all species investigated (Fig. 4.1, 4.2; Table 4.1). Adductor muscle CSA has been

shown to be one of the most common predictors of bite force in sharks, clariid fishes, and bats

(Dumont et al., 2002; Herrel et al., 2007; Habegger et al., 2012).

Clear predictors for posterior bite force (PBF) were not detected in the analyses. The fact

that the intercept-only model (with no predictors) ranked above all other models indicates that

none of the variables explored may be a particularly useful to predict PBF. Although the lack of

clear predictors has been described for other taxa including alligators (Erickson et al., 2012), a

possible reason for these results could be the large variability associated with measuring the most

posterior tooth position. In swordfish, the teeth are reduced to almost absent making the most

posterior position difficult to determine. However this variability does not prevent further

comparisons in biting performance overall, given that most comparative analysis in fish, both

theoretically and experimentally, are more likely to use ABF over PBF because it is accessibility

(Huber et al., 2005; 2009, Mara et al., 2009, Grubich et al., 2012).

Mechanical advantage (MA), a variable used to characterize closing performance of the

lower jaw can also influence bite force. Mechanical advantage of the jaw adductor mechanism is

indicative of the trade-off between two performance measures, force and velocity (Westneat,

98

2004). High MA resulted in the amplification of biting performance in the chimaera (PBF=190

N) (Hydrolagus colliei) (Huber et al., 2008), horn shark (ABF=382 N) (Heterdodontus francisci)

(Kolmann and Huber, 2010) and is an important predictor of size specific bite force throughout

shark evolution (Habegger et al., 2012). The low AMA in billfishes and the wahoo (0.25-0.27) is

characteristic of fishes reported as having a speed efficient, rather than force efficient jaw

(Westneat, 2004).

Bite force comparison

Even though bite force varied among billfishes, when comparing biting performance to

other fishes, the pattern is clear. Billfish showed overall low values of relative bite force

compared to “non-billfish” species of similar ecology, supporting one of my hypotheses (Table

4.4). High bite forces does not appear to be crucial for billfish predatory success. Although the

rostrum cannot be definitively categorized as an adaptation for feeding, its use has been shown to

enhance prey pre-processing (Domenici et al., 2014), perhaps reducing the need for strong bite

forces relative to other “non- billfish” species. Numerous top predators have been shown not to

rely on large bite forces for prey capture and processing. For example, the great barracuda

(Sphyraena barracuda) and the king mackerel (Scomberomorus cavalla), seem to rely in a

combination of high pursuit acceleration, fast jaws and sharp teeth to capture and subdue their

prey (Habegger et al, 2010; Ferguson, 2014).

Bite force is often related to prey properties; for example, turtles (Chelydra and

Staurotypus) and lizards (Anolis sp.) that eat harder prey showed higher biting performance

(Herrel et al., 2001, 2002). However, dietary preferences are highly conserved among billfishes;

and their diets are composed mostly of teleost fish such as scombrids and carangids, as well as

99

Reduction in eye size in Petrotilapia resulted in a concomitant increase in jaw adductor muscle size (Barel. 2011). 100 . In mouthbrooding cichlids (Haplochromis) an increase in mouth size to accommodate larger egg masses affected biting performance imposing a trade-off between the two fitness parameters (tkint et al. trade-offs imposed by locomotion constraint biting performance (Vanhooydonck et al. In billfishes. Whitenack et al. In the burrowing skink (Acontias percivali). In addition the force needed for shark teeth to puncture fish prey is surprisingly low (5 N. 2012) suggesting that in billfish high values of bite force may not be essential.. 1993). the area where the adductor musculature usually resides maybe under competing functional trade-offs. blue marlin stomach contents showed lacerations mostly in larger prey sizes (Katsuwonus pelamis >150 mm) (Shimose et al. 1983). Low values of bite force in billfish could be attributed to functional trade-offs between feeding.. mostly squid (Nakamura. The heating organ.cephalopods. whereas processing of hard prey such as turtles shells may reach significantly larger values (up to 3000 N) (Macwene and Socha. obs. and for instance sensory structures in the head or hydrodynamics. 1997). generating heat and possibly augmenting vision (De Metrio et al. 1985. 2009). 2007).) resulting in the lower biting performance. 2007) suggesting the rostrum may be used for processing larger prey.. one of the characteristics of this group (Block. Finally... is formed from a modification of the dorsal rectus eye muscle. 2012). Shimose et al. A large amount of adipose tissue surrounding the eyes may limit the available space for the jaw adductor muscles (Habegger pers.

2004). 1983. and striking in any plane for the blue marlin (Chapter 2). 1974. had both the lower and upper jaw elongated (Fierstine. Stunning prey with both elongated upper and lower jaws could create constraints on breathing by limiting flow into the mouth and through the gills. Paleorhynchus and Xiphiorhynchus. however. it has been suggested that a short rostrum is the ancestral condition for the group (Nakamura. 2006). and breakage of both jaws during prey striking or defensive behavior could result in total incapacitation for prey capture (Fierstine. However. The ancestral rostral condition for this group remains unclear. Johnson.. Webb. Fierstine. 2014. In addition to striking prey. the rostrum may decrease drag during feeding. most of the basal extinct species of billfish. has been shown to trigger prey awareness (Dill. Chapter 2). such as Aglyptorhynchus. it may reduce the chances of early detection and fleeing by prey when approached head on as the rate of angle change of a predator’s frontal profile. In addition. Contrary to many other predators with long jaws. Theoretical models indicate drag is lowest during lateral striking as compared to dorsoventral striking in swordfish. Recent field observations and mechanical testing support the idea that this novel structure acts as a feeding weapon and that rostral morphology may influence feeding behavior (Domenici et al. Long and narrow rostra or jaws result in a less abrupt 101 . 1999) with subsequent changes in length through evolution to facilitate feeding. The loss of the elongated upper and lower jaws may be related to the feeding behavior in billfishes. 1982). several aspects indicate feeding as one of the most plausible explanations (Fierstine. 2006). billfish only have their upper jaw elongated. 1986. 2006). the “looming threshold”. such as gar (Lepisosteus platyrhincus) and needlefish (Strongula notata) that capture elusive prey with rapid jaw adduction (Porter and Motta.Rostrum evolution The role of the rostrum in billfishes has been controversial for decades and although its adaptive value cannot be assured.

Even though there was no association between rostrum length and bite force production within billfishes. their predatory success may reflect a combination of many variables including elongation of the rostrum to capture and process prey. results suggest that rostral elongation may relax the selective pressures towards high biting performance. 102 . In summary bite force performance within billfishes was predicted by adductor muscles CSA and was not related to rostrum length. Similar to other apex predators. Although the rostrum of billfishes has yet to be established as an adaptation for feeding.change in frontal profile of a predator as they approach a prey and fleeing by the prey might be delayed until the predator is within striking distance. it is clear that billfishes do not rely on extreme bite force as apex predators.

(2010). (2014). 103 . (1986). C. Heat-Producing Organ of the Swordfish (Xiphias gladius): A Modified Eye Muscle. Ditrich. N. D.References Arnold. G.. glmulti: an R package for easy automated model selection with (generalized) linear models. T. Journal of Morphology 234. San Luis Obispo.N. C.D. Springer-Verlag. 53. California Polytechnic State University. J.. Barel. G. and Goldschmidt. An illustrated study of the feeding mechanism of the Blue Marlin (Makaira nigricans). Zool. (1983). Atkins. Zool. Model Selection and Multimodel Inference.T.. Anderson. Softw. (1997) Model selection: An integral part of inference.. Remodeling of anosteocytic bone. C. S. Anker. R. Bloomer. New York.C. Barel. Buckland... Constructional 581 constraint and its ecomorphological implications. and Palmieri. Form-relations in the context of constructional morphology: the eye and 575 suspensorium of lacustrine Cichlidae (Pisces.P. 34. and de Mazancourt. Nat.. (2008). R. Teleostei): with a discussion on the 576 implications for phylogenetic and allometric form-interactions. 23: 347-361.L. Calcagno. Biometrics.R. C..J. De Metrio. Witte. and Shahar. (1984). performance and fitness. 603-618.89-96.H... Augustin. Motta.R. (Unpublished senior project).J. Springer.D.N. Stat. Acad. Burnham.J. and Anderson. J. (2002). A. D. (1989). Hoogerhoud. Amer. J. Sci. Currey. 34. F. C. P. Proc. K. Burnham. (1997).439-577 502. Dean. V. Morphology. Model Based Inference in the Life Sciences. i12. Acta Morphol Neer Sc 27:83-109. Habegger. M. S. K.C.P. M. H. Neth.

. Ferrara.. P.E. 22..M.. Couillaud. K..M.. Achaval. The effects of gape angle and bite point on bite forces in bats.. E.C. H. J. P. University of South Florida. A. Fish.2014. Steffensen. Verraes..S.M.Devaere.org/10.. D..P.. Glannakis.C. How sailfish use their bills to capture schooling prey. S. Y.M. Domenici. Grafen. The phylogenetic regression. Teeuwisse.L. 85-96. Cranial morphology of the anguilliform clariid Channallabes apus (Günther.G.. Chelonia: Cheloniidae and Dermochelyidae) by billfishes (Osteichthyes. 119-157..L. Ferguson. S. 710-721.. (2003). Env.. S. Fry.. Wilson. E.L. Thesis.. Biol.. K. Soc. Scanlon. P. Hodgson. Viblanc.H. A. (2014). T. Luz. van Osch. Martelli.. Beavers. S. Karas. R. Adriaens. J.E.. (1989). P. Trans. Yamaguchi.F. Biol. A. E.J. Kurvers. M. Roy.. H. S.... D. Ingle. (2001). The stimulus for escape. Kwok..0444.. (2014). Krishnasamy.M. Frazier. Exp. 104 .. J. C. Fierstine. Goldstein. 8969-8974.1098/rspb. 255.. Dumont. J. D. W. 1873) (Teleostei: Siluriformes): are adaptations related to powerful biting? J. J. (1994). and Teugels.G.R. R... Marras. Hiroyuki. B. P. Wroe. W. B 326. McHenry. Scheib.. C. Kochva. H.. A. 206: 2117-2123. J. Feeding performance of king mackerel. Zool.dx. McNaughtan. Scomberomorus Cavalla. Soc. (1974). and Prigioni.. E. R. J. J.. W.J. A. Dill. Philos. 39. Anim. Citron.(2009) A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus..G. Pitman. Perciformes: Istiophoridae and Xiphiidae). Behav. S. and Norman.D. Krause. Winter.. S. and Herrel. and Krause. Moreno. Clausen.doi. 106. The escape response of zebra danio (Brachydanio rerio).235-250. L. Impalement of marine turtles (Reptilia. K.. Herbert-Read. S. E.. G. M. Proc.J. F. PNAS.

(1996). Motta.. 27: 501-542. Biol.. 9-12 August 1972. Herrel.F.. Bengal Branch. Exp. Soc. J. Lemos-Espinal.J.C. A. J. 105 . & Motta. J. Rev. 1914 in the Indo-Pacific areas. 737-756. P. Zool. J. J. Copeia 2006(7). Mem. The allegated pugnacity of the swordfish and the spearfishes as shown by their attacks on vessels. (2001).669-675. Husak. J.R.L. E. P. 15. 18. J. J. D. Herrel. (2006). Lemos-Espinal. and Hendry. Syst.P.. Kumar. Evol. Bite. 2971-2972.G. 101-107. (1997)... Hawaii. Huber. Ecol. Asiatic. O’Reilly. E. 3553-3571. M. Herrel. Kikawa. Hueter. Trophic consequences of differential performance in the sheepshead. Analysis of bite force and mechanical design of the feeding mechanism of the durophagous horn shark Heterodontus francisci.Gudger. S. K. A. 290. Biol. S. 39-54. Evolution of bite force in Darwin’s finches: a key role for head width.M. Synopsis on the biology of the Shortbill Spearfish. S.W. Kailua-Kona. Sparidae).. Podos.E... Huber.. J. L. Hedges. Archsargus probatocephalus (Teleostei. (2002). Tetrapturus angustirostris Tanaka. 243.A. Head shape and bite performance in Xenosaurid lizards.R. Procceedings of the International Billfish Symposium. Dudley. De Grauw. (1975). S. (2005). S. Eason. T. 301- 306.P. Bioinformatics 22. Koehl. A.A. (2005). Exp. Evol. 1083-1094.A. Biol. 2. J..force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus).F. Hernandez.K. and Richmond. Roy. Zool. R. A. Fox. (1940). Evolution of bite performance in turtles.. Lappin. A. 208. 215-31.. (2006) TimeTree: a public knowledge-base of divergence times among organisms. When does morphology matter? Ann.B.

Res. S. Saito. Tachihara.. 25. 217-223.. Shimose. Res. (2009) Size-Correction and Principal Components for Interspecific Comparative Studies. 213-233.N. Zool. nlme: linear and nonlinear mixed effects models.J. J. and Tawara.html). Pinheiro. DebRoy. (2004). F. APE: an R package for analyses of phylogenetics and evolution. Fishing condition of tuna and marlin in the central south Pacific.org/ web/packages/nlme/index. Revell. Ichtyol. (2001). 3258-3268. Systematics of the billfishes (Xiphiidae and Istiophoridae).J. Statistical approaches to the problem of phylogentically correlated data. and Sorenson. 481-489. Canada. Revell. Santini. Publ. I. F. S. Food and feeding habits of swordfish.r-project. Lab. Biol. S.Koga. E. 2143-2160. M. (1983). Ital. Scott. 903-972. R package version 3. H. (2013). J. L. K. Imanishi. Comparative methods for the analysis of continuous variables: geometric interpretations. 80. K. First molecular timetree of billfishes (Istiophoriformes: Acanthomorpha) shows a Late Miocene radiation of marlins and allies. Rohlf. in theWestern North Atlantic.A. Shimonoseki Coll. 255-396. W. 28. Evidence for the use of the bill by blue marlin (Makaira nigricans). Lajeunesse.1-86. (1972). In Prep. S. Bd. Fish 20. Claude. (1968). J.. during feeding. D. Nakamura.. Strimmer. K. and Sarkar.J. M. Jour.. (2007). Bates. (2012) phytools: an R package for phylogenetic comparative biology (and other things). J. T. and the R Core team. Methods in Ecology and Evolution 3.B. L. L.. Seto Mar.. (2007). Fish. 289-290. and Tibbo. Bioinformatics 20. (http://cran.. 106 . Xiphias gladius. Evolution 55. 54. Yokawa. D. Evolution 63. 420-422. Paradis.

55. 126-137. Sci.. Dissertation.J. Relationships between head size. U. T. Commerce SSRF-675. (2012) Dealing with Food and Eggs in Mouthbrooding Cichlids: Structural and Functional Trade-Offs in Fitness Related Traits. and Herrel. 125. bite force. 468. (2010).1371/journal. and Tachihara. Ecol. (2008). R. Ichthyol.. The Biomechanics and Evolution of Shark Teeth. A descriptive synonymy of the striated muscles of the Teleostei. K.S. Proc. F. Ph. Istioampax marlina. R. L. 16. around Yonaguni Island.0031117. fifth edition. Acad.H. Fish. Saito.. Serv. Rep. Biostatistical analysis. (2009). Length-weight relationships for six species of billfishes in the Central Pacific Ocean. 225-317. University of South Florida. Zar. southwestern Japan.pone. tech. 842-850. Verwaijen. prey handling efficiency and diet in two sympatric lacertid lizards. Verheyen.. Funct. J. (1974). K. Prentice Hall. Skillman. Van Damme. J. B. M. Dep.Shimose..A. and Penrih.. De Kegel. Res. Whitenack. 107 . E. M. Spearing behavior in feeding in the black marlin.D. (1974). Phila. and Yong. tkint. T. Adriaens. Helsen. Winterbottom. D. PLoS ONE doi:10. Talbot. mar. Seasonal occurrence and feeding habits of black marlin (Istiompax indica). (2002). Copeia 1964. D. A. 90-94..A. P.H. Yokawa. R. NOAA natn. Nat. (1964).

85 Tetrapturus albidus 7 78.57 ± 0.28 22.09 3.56 ± 0. A3= cross sectional area of the subdivision of the adductor muscles 108 .6 ± 0. AOL=anterior out lever.1 20.12 ± 0.46 48.43 ± 1.47 0.71 ± 0.74 2.39 8.43 ± 4.6 ± 1.01 1.23 ± 62.48 18.33 ± 0.69 Xiphias gladius 7 56.7 ± 14.09 ± 2.01 1.32 18.1 10.34 ± 1.29 10 ± 0.9 ± 1.6 1361 ± 184.9 29.84 ± 1.76 49.9 ± 1.12 6.32 0.59 5.68 ± 0.57 ± 2.05 ± 2.78 405.76 ± 0.73 0.66 ± 0.44 ± 7.22 ± 6.02 0.54 29.55 158.45 ± 0.26 ± 0.5 15.98 ± 19.92 9.27 ± 0.25 ± 0.33 ± 0.16 98.26 ± 0.2 ± 0.67 331.92 1.46 4.15 8.0 218.79 ± 0.95 Istiophorus albicans 3 60.93 ± 0. POL= posterior out lever.13 ± 3.06 25.62 ± 3.62 ± 0.26 ± 0. PBF= posterior bite force.6 6. solandri).5 6. BL= bill length.73 ± 10.86 ± 1.21 0.27 ± 0.46 0.39 0.73 80.3 38.74 ± 0.52 15.06 4.21 3.1 ± 2.35 ± 7.17 23.38 ± 1. AMA= anterior mechanical advantage.97 ± 38.24 ABF=anterior bite force.4 72.Table 4. Raw mean values ± SD of bite force and biomechanical variables for billfishes and wahoo (A.83 ± 48. A1+A2= cross sectional area of the subdivision of the adductor muscles. IL= in lever.24 ± 0.05 ± 0.77 4. BITE FORCE SPECIES INFORMATION BIOMECHANICAL VARIABLES SPECIES N ABF (N) PBF (N) Mass (kg) BL (cm) AMA PMA IL (cm) AOL (cm) POL (cm) A1+A2 CSA (cm2 ) A3 CSA (cm2 ) Acanthocybium solandri 6 29.54 ± 0.97 ± 0.44 2.02 0.37 ± 3.14 5.53 205.0 1.67 ± 0.18 ± 10.03 6.94 Tetrapturus angustirostris 5 37.64 24.97 ± 40.68 ± 0.09 7.25 ± 0.87 Makaira nigricans 6 329.61 1.1.84 ± 16.3 ± 0.8 4.52 ± 40.15 6.0 1.05 ± 0.43 ± 31.96 29. PMA=posterior mechanical advantage.17 ± 0.5 41.84 ± 1.97 ± 0.

99 33. All models include the intercept.65 0.35 0.0011 PGLS 2 ABF~ 1 + IL 21. The statistical significance of the predictors included in regressions are also presented (F-tests). Models that have no variable (e.98 2.35 0.1640 Posterior bite force PGLS 1 PBF ~ 1 25.61 0.03 0.0514 PGLS 4 PBF ~ 1 + PMA 27.0399 Model selection of predictors based on  AICc equal or lower than 2.78 7. ABF ~ 1) indicate an intercept-only model with no predictors. 109 .99 0.56 0.00 0.34 0.0 (emphasized in bold.22 3.06 0.97 2.67 0.47 0.0310 PGLS 3 PBF ~ 1 + AOL 27.95 9. the results of these significance tests were not used during the model selection analyses.79 4.01 0.=1) weights Anterior bite force PGLS 1 ABF ~ 1 + A1+A2 17.13 0.35 NA NA OLS 2 PBF ~ 1 + A1+A2 17.2.09 0.61 0.0638 OLS 4 ABF ~ 1 AOL 24.g.74 2.16 0.43 NA NA OLS 2 ABF ~ 1 + A1+A2 19.30 0.94 0.25 0.11 0.00 0.89 0.99 4.76 69.43 0.88 3..87 6.76 0.f.99 0.13 0.0288 OLS 3 ABF ~ 1 + IL 21.41 0.66 0. Model selection of bite force predictors based on AICc values among billfishes and wahoo (A.53 11.95 6.0036 PGLS 3 ABF ~ 1 + AOL 21.30 0.0649 PGLS 5 PBF ~ 1 + A3 28. Phylogenetically-corrected regressions were based on PGLS analyses assuming a full Brownian motion model of evolution.89 37.24 1.12 0.13 0. cum.35 NA NA PGLS 2 PBF ~ 1 + A1A2 25.81 1.71 5.73 0.0043 OLS 1 ABF ~ 1 19.00 0.67 0.34 0.97 3.62 0. following Burnham and Anderson 2002). also presented are models with minimal support with  AICc values < 7. Regression Best fit AICc F Best fit models AICc  AICc AICc p model rankings weights (d.0.Table 4.0865 PGLS 6 PBF ~ 1 + IL 28.49 0.59 0.67 0.93 5.57 0.13 0.65 10.10 0.00 0.06 0.0892 OLS 1 PBF ~ 1 16.06 0.14 0.40 0. and conventional regressions were based of OLS models without phylogenetic correlations. solandri).

57 ± 2.07 0. 110 .05 37.28 0.70 56.03 -0.67 -1.2 Xiphias gladius 7 41.1 All values are from anterior bite points.73 ± 10.6 0.84 ± 16. Species are organized from smallest to largest size-corrected bite force.97 ± 40.Table 4.07 Makaira nigricans 6 218. Mass specific bite force (mean ± SD) within billfishes Size corrected Phylogenetically SPECIES N Mass (Kg) Absolute ABF (N) residulas corrected residuals Istiophorus albicans 3 20. residuals are mass specific bite forces and phylogenetically corrected residuals are relative values of bite force corrected for the lack of independence among species.52 329.16 0.43 60.55 0.96 1.03 -0.3.98 Tetrapturus angustirostris 5 15.34 78.32 -0.62 ± 3.53 -0. ABF= absolute bite forces for each species.18 ± 10.22 29.1 Tetrapturus albidus 7 29.05 Acanthocybium solandri 6 18.78 0.

ABF= absolute bite forces for each species.7 56.5 330.Huber et al.7 19. residuals are mass specific bite force.3 68.30 Great barracuda2 Sphyraena barracuda 4 14. (2006) 5.Habegger et al.Ferguson.5 81 -0. were gathered from the literature cited bellow.6 -0.42 Shortbill spearfish Tetrapturus angustirostris 5 15. Mass specific bite force in billfish vs “non-billfish”.35 White marlin Tetrapturus albidus 7 29.51 Wahoo Acanthocybium solandri 6 18. Durophagous taxa are not included 1.16 Lemon shark3 Negaprion brevirostris 4 1.4 60.Table 4.. Common name Scientific name N MASS ABF Residuals Blue marlin Makaira nigricans 6 218. (2012) 111 . Non- billfish species except for wahoo.4.65 Bull shark5 Carcharhinus leucas 4 91.09 Blacktip shark4 Carcharhinus limbatus 4 7.5 0..6 -0.87 All values are from anterior bite points.2 -0. (2010) 3.6 -0..30 Sailfish Istiophorus albicans 3 20.7 -0. (2005) 3.36 Kingfish mackerel1 Scomberomorus cavalla 7 5.8 -0.5 2.73 247.Habegger et al.2 29.3 -0.1 907.1 37.39 Swordfish Xiphias gladius 7 41.Huber.0 -2. (2014) 2.3 78.

1. nigricans. . 4. gladius. albidus and a non-billfish species used as the outgroup (wahoo.Fig. Tree topology was based on Santini and Sorenson (2013). 112 . A solandri). albicans and white marlin T. and internode branch-lengths were based on known divergence times reported by Hedges et al. sailfish I. Phylogenetic relationships among five billfishes species (blue marlin M. Outline figures were modified from Diane Peebles. shorbill spearfish T. (2006). swordfish X. angustrirostris.

Mx= maxilla. solandri).Fig. Outline of the adductor mandibulae complex (superficial subdivision A1+A2) in three representative billfishes (complete rostrum not shown) and wahoo (A. solandri). Pop=preopercle. B) Adductor mandibulae subdivision A1+A2. OP= opercle. D) Adductor mandibulae subdivision A1+A2. gladius). angustrirostris). Sop= subopercle. Aw in the shortbill spearfish (T. D=dentary 113 .2. C) Adductor mandibulae subdivision A1+A2. PMx=premaxilla. Aw in swordfish (X. Gregory and Conrad (1937) for swordfish and Conrad (1938) for wahoo. Outlines were modified from Bloomer (1986) for blue marlin. 4. Aw in the blue marlin (M. nigricans). Aw in wahoo (A. A) Adductor mandibulae subdivision A1+A2.

A) Adductor mandibulae subdivision A3 in the blue marlin (M. Subdivisions A1+A2 and Aw not shown. angustrirostris). C Adductor mandibulae subdivision A3 in swordfish (X. Outline of the adductor mandibulae complex (deeper subdivision A3) in three representative billfishes (complete rostrum not shown) and wahoo (A solandri). B Adductor mandibulae subdivision A3 in the shortbill spearfish (T. 4. D Adductor mandibulae subdivision A3 in wahoo (A. Outlines were modified from Bloomer (1986) for blue marlin. Gregory and Conrad (1937) for swordfish and Conrad (1938) for wahoo. gladius). nigricans).Fig. 114 .3. solandri).

nigricans) and white marlin (T. From top to bottom (lowest to highest relative bite force): sailfish (I. 4. blue marlin (M.Fig. albidus). angustrirostris). 115 . solandri). Black bars show residual values of bite force performed in a linear regression. shortbill spearfish (T.4. albicans). Relative bite force within billfish and outgroup wahoo (A solandri). wahoo (A. swordfish (X. Grey bars show phylogenetically corrected residuals generated following Revell (2008). Residuals values range from negative (lowest) on the left to positive (largest) to the right. gladius).

but also in relative lower jaw length. not only in rostrum length. However the acquisition of new structures can be costly. limiting structural space and therefore sometimes jeopardizing organismal performance. most of the variation was found between blue marlin and shortbill spearfish. Billfish 116 . A total of 55 landmarks were positioned along the skull of five billfish species and wahoo. CHAPTER FIVE GEOMETRIC MORPHOMETRICS OF THE BILLFISH SKULL Abstract Feeding has been perhaps one of the major drivers of skull diversification. offering a good opportunity to investigate how changes in rostrum morphology could influence skull variation. and the possible implications of rostral morphology in billfish feeding performance. This novel structure utilized as a feeding weapon is morphologically variable within the group. swordfish had an abrupt reduction in all skull dimensions and an elongation of the rostrum. Novel structures have augmented this diversity by offering raw material for evolution. In this chapter I conducted a comprehensive three dimensional analysis of skull and rostral morphology for this phylogenetically diverse group (Xiphiidae and Istiophoridae) in order to investigate potential trade-offs in cranial architecture. Warping analysis showed most of the variation to occur between swordfish and istiophorids. Billfish are a group of large apex predators characterized by the elongation of their upper jaw. Within istiophorids.

Hall.species with relatively large rostrums have relatively short lower jaws. showed an abrupt reduction of the skull length.. The possible implications of this variability are discussed in an ecological context. the skull has apparently played a crucial role in vertebrate radiation (Cole and Friedman. No trade-offs were found between eye size and muscle size. Feeding has been perhaps one of the major drivers of skull diversification. skull length and width. and eye size was conserved despite muscle size varying among species. In fishes in particular. and housing sensory organs. 1990). suggesting that eye size may be under stabilizing selection. The shortbill spearfish showed opposite patterns with a relative increase in lower jaw length. The variability found in the feeding morphology of fishes reflects their wide range of food capture methods from suction to ram feeding (Ovchinnikov. height and width. respiration. 1970). Takahashi et al. Organismal diversity can be amplified by the occurrence of novel structures as evolutionary novelties provide the raw material for natural selection to act on (Jablonski. In conclusion. 2012). 117 . as illustrated by the enormous diversity found in the rostral and oral regions of vertebrate skulls (Schwenk. 2005). perhaps suggesting differences in feeding performance associated to morphology. 2005). Swordfish. Additionally the lower jaw was also reduced. the majority of morphological variability in the billfish skull resides in upper and lower jaw length and changes in skull height. this diversity is remarkable owing in part to the fact that they represent almost half of all living vertebrates (Nelson. 2007). the species with the longest rostrum. as well as their dietary diversity ranging from herbivory to scale eating (Westneat 2006. With roles in feeding. Introduction The skull of vertebrates is a complex integrated structure involved in several important functions for organismal survival. 2000.

1962).g. However. and surfperches) (Liem. 118 . Olson et al. Dumont et al. Trade-offs have been suggested in other systems with novel structures. Probably one of the most investigated novelties in fishes is the pharyngeal jaw apparatus in labrid fishes (cichlids. for instance. (2005)]. 1988. or genetics [e. novelties may emerge from the modification of simple structures resulting in novel functions as exemplified by the highly kinetic beak of birds that resulted in an amplification of feeding function unique to this group (Beecher. In addition. eye volume is reduced in some species with the enlargement and consequent thinning of the cephalofoil (Mara. (2005)]. 2010) and also in specialized feeders such as mucous eating fish (Labridae) where force efficient jaws have limited speed (Bellwood et al.... 2012). Mulvany and Motta. parrotfishes. damselfishes. suggest trades-off that favor force production (Devaere et al. with the concomitant reduction in the associated areas of the skull. 1991). weed whitings... The enlargement of the adductor muscles in catfish. wrasses.. Price et al. The pharyngeal apparatus acts as an independent set of jaws allowing for a functional decoupling from the oral apparatus resulting in an immense trophic diversification (Wainwright et al. skull variation and bite force production in mammals lead to niche diversification. 2010). 2001). Many labrid species have a fusion of some ceratobranchials that significantly reduces the size of the pharyngeal gape. 2006).g. 1973. which generates a trade-off between prey size and prey type consumption (Wainwright. behavior [e.g. the cephalic lobes in batoids allows decoupling from locomotion and feeding thereby increasing maneuverability. in the hammerheads sharks (Sphyrnidae). Wainwright. some innovations may come with an associated cost. Dlx genes giving origin to vertebrate jaws. while these novelties may amplify diversity.Novelties may occur as a product of changes in morpho-functional complexes [e. (2013)].

.. Domenici et al. chondrostean paddlefish). 2014). Bite force has been linked to skull architecture and size. Dewar et al. Fierstine 1997. Habegger et al. Herrel and O’Reilly. and concomitantly there may be trade-offs between cranial volume and shape.. Fierstine. Talbot and Penrith. Davie... fast swimming speeds and their important value in fisheries (Nakamura. the role of the rostrum is still debatable. 2003. consequently limiting biting performance. in paddlefish (Polyodon sphatula) the “paddle” is composed of elongated rostral cartilages (Furimsky et al. 1996). belonid needlefish.g. Shimose et al. 2013). 2012). and adductor size. Although rostral elongation is not unique to billfishes (e. 2014). 1990.. 1962. 1990. head length and width. material properties. Wider heads have more space to accommodate large adductor muscles that can produce extremely large bite forces as seen in alligators and bull sharks (Ericskon et al. eye size. or the skeletal elements involved in rostral elongation may differ. Although this group has been intensively studied because their migratory patterns. wider heads may come at a hydrodynamic price for cruising specialist fishes. Fierstine and Voigt. 1985. However. Wainwright 1987. It has also been suggested that its role in capture and processing may have resulted in the release of selective pressures for high bite force (Chapter 2). Bite force is often used as a window to feeding performance and ultimately fitness. in 119 . 1984. 1940. For example. the general developmental pattern. and head depth. Previous studies have shown this novel structure may be used in feeding. Sagong et al. and has been established as a good proxy for biting performance (Carothers. both to assist in capturing prey and also to process it by cutting it in pieces before ingestion by the oral jaws (Gudger. the extension of several cranial bones that constitutes the rostrum (Nakamura. 2006). 2011. 1985. Billfishes are named after their most conspicuous attribute. 2007..

Lavejoy et al. information on the correlated changes or possible trade-off between rostral elongation and skull morphology have been less investigated [but see Kulemeyer (2009) in birds. Billfishes present a great opportunity to evaluate the correlated changes or possible trade- off between rostral elongation and skull morphology and performance for many reasons: the morphology of the rostrum and the skull varies among species not only in shape. The skull in istiophiorids is stouter and wider than in xiphiids for which a lower level of ossification has been reported. particularly in swordfish which have been suggested to be highly visual predators (Fritsches et al. Although the anatomy and development of these structures are somewhat well known (Collete et al. offers an opportunity for the utilization of a 3-dimensional morphological analysis generally not possible in smaller fishes. 1984. Atkins et al.. The rather small number of species in this group allows the possibility for a comprehensive comparative analysis.. 1983). (2012) in rodents]. but also in length ranging from up to 50 % of body length in swordfish to only a few cm in length in the shortbill spearfish (Tetrapturus angustrirostris) (Nakamura. 2014. 2005). in some species up to 4 m in total length and 500 Kg (Nakamura. Gunter et al. Finally. the availability of other biomechanical performance measures including bite force. Chapter 2. Eye size in billfish is large. jaw lever mechanics. muscle cross sectional area. 2014)... and Hautier et al. whereas in needlefishes (Belonidae) both jaws are elongated (Gunter et al. 1983).. and their large size. ranging from elliptical in cross section in swordfish (Xiphias gladius) to round in istiophorids such as blue marlin (Makaira nigricans). 4) allow the investigation of other possibly correlated characters 120 . 1985)... 2014). and rostrum biomechanics (Atkins et al. (2010) in pipefish. 2004. 1991.. 2014. Boughton et al. within istiophorids the skull is also variable in size and shape (Nakamura.halfbeak fishes (Hemiramphidae) their “beak” is a result of elongation of the lower jaw. Leysen et al.

Scans were performed with a GE 64 slice Lightspeed CT scanner. (1990). The goal of this study is to conduct a comprehensive three dimensional analysis of skull and rostral morphology for a phylogenetically diverse group (Xiphiidae and Istiophoridae) of billfishes in order to investigate potential trade-offs in cranial architecture. with a slice thickness of 0.625 mm. Gudger (1940). as well as pictures from 121 . Nakamura (1983). N=3). and the Atlantic sailfish (Istiophorus albicans. following anatomical descriptions from Gregory and Conrad (1937). N=4). Three dimensional reconstructions from CT scan data were made in Mimics software (Materialise HQ. N=4). N=4). Davie. the wahoo (Acanthocybium solandri. N=4).to cranial morphology. shortbill spearfish (Tetrapturus angustrirostris. To evaluate the results through phylogeny an outgroup species. Billfishes species collected ranged widely in size (13-270 Kg). Fierstine et al (1990). and the relationship of biting performance to rostral morphology. was also included following the latest billfish phylogeny by Santini and Sorenson (2013). N=3). All heads were kept frozen until CT scanning was performed. rostrum morphology (rounded to elliptical in cross section) and length (20-90 cm from distal end of the rostrum to the beginning of the orbit and) and are intended to encompass a wide range in phylogenetic positions based on their availability. white marlin (Tetrapturus albidus. Species utilized in this study were swordfish (Xiphias gladius. the east coast of USA and Hawaii. blue marlin (Makaira nigricans. Belgium). Materials and methods Landmarks description A total of 22 specimens from five billfish species and one scombrid species were collected from recreational fishing tournaments and commercial fisheries along the Gulf of Mexico.

rotation and translation of the landmarks around a centroid. Landmark analysis All landmarks were imported and superimposed by performing a Procrustes Analysis Generalized Least Square (PGLS) to EVAN geometric morphometric toolkit (EVAN‐Society. and that some specimens had their jaws open during scanning while others were closed. semi- landmarks were utilized as points that delimited a particular structure such as the rostrum or the sclerotic bones. Closure was accomplished first by isolating the lower jaws from the skull in Mimics and rotating them in 3-Matics (Materialise HQ. Ichthyology collection and skeletonized skulls. Austria). 5. the lower jaws of the open specimens were digitally closed in the rendering. University of Vienna.1). This method allows shape comparison among individuals after scaling. Accounting for the fact that the 3-D coordinates were highly dependent on the anatomical position of all skeletal elements of the skull. A total of 55 three-dimensional landmarks were used (Table 5. Belgium) via point registration. or on the widest and highest positions. Once the position of the jaws was repositioned the landmarks were digitized. such as along the sclerotic bones (Fig. However. Shape 122 .1). To account for size regression of Procrustes coordinates against centroid size were performed. Semilandmarks were positioned equidistantly along each surveyed structure such as the rostrum. In most cases landmarks represented homologous anatomical points on evolutionary stable structures among species. Vienna. in some cases where these anatomical landmarks were not clear.skulls at the Smithsonian Natural History Museum.

These PGLS analyses were fitted using the gls() function from the nlme package (Pinheiro et al. A full Brownian motion model of evolution was assumed for all PGLS analyses because of the low sample size (N = 6) necessary to estimate lambda-fitted (phylogenetic signal) models. All data were size-corrected by weight using the phylogenetically-corrected method outlined by Revell (2009) and implemented in the R package phyTools (Revell. adductor muscle cross sectional area (AM=CSA A1+A2. Variables utilized on this analysis where head width at four different areas of the skull (HW1= distance between O1-O5. 1985). HW4= O2-O6). lower jaw length (LJL=M1-M2).5. consequently pairwise comparisons were performed for the raw data and phylogenetically corrected data. 2012). IL) (Chapter 4..). Size-corrected trait values were then analyzed using phylogenetic generalized least squares (PGLS) regressions following Revell (2009) assuming trait evolution via Brownian motion (Grafen. Belgium) and linear regressions and pairwise correlations were performed in R. Rohlf 2001). HH2= M2-H5). data points are not independent (Felsestein. and lever arms. 17 linear dimensions of these variables were gathered from CT scan data in Mimics (Materialise HQ. 2007) assuming a maximum likelihood estimator (ML) and a 123 . eye size (SCL=Sc1-Sc3. HW2= H7-H8. After proper identification of the variables that contributed to most of the shape variation among billfish skulls either from PCA or warping analysis.1). head height (HH1= M2-Ep1.variability was then analyzed by principal component analysis (PCA) with and without size as a variable and by qualitative observations from warping analysis. As all billfishes share a common history. lower jaw width (LJW=M2-M3) (Fig. 1989. HW3=S1-S2. AM2=CSAA3). head length (HL=R1-Ex1). and from a previous study anterior bite force (ABF). as well as anterior mechanical advantage and in-lever (AMA. rostrum length (RL=R1-O1). SCH=Sc2-sc4).

The relative size of the swordfish suspensorium was also reduced. (2006).. The reduction of the dorsal portion of the hyomandibula is reflected in the overall reduction of the posterior region of the skull. The skull of swordfish demonstrated reduction in relative length.Brownian correlation structure defined by the corBrownian() function from the ape package (Paradis et al. Fig 5. height and width compared to those of all istiophorids.8. 2004). The slope of the each regression was estimated as well as the correlation of the traits through a Pearson correlation (r). 124 . The phylogenetic tree (Fig. 5. In addition all the posteriorly located processes of the epiotic and pterotic that are elongated in istiophorids are reduced and blunt in Xiphias (Fig. where the hyomandibula articulates with the sphenotic and pterotic bones.1. Results Warping: qualitative analysis of the major trends in the skull of billfishes Overall patterns of shape variation were more conspicuous between the swordfish and the istiophorids. This was performed for the raw data (red slopes when regression was significant) and the phylogenetically corrected data (blue slopes when regression was significant).3). especially at the dorsal portion of the hyomandibula. regardless of species. Results were plotted in a large regression-correlation matrix and patterns identified and reported by first isolating the regressions with significant slopes and then the correlation value (r) larger than 0. 5.2) used in size-corrections and phylogenetic analyses had a topology based on Santini and Sorenson (2013) and internode divergence times based on Santini and Sorenson (2013) and Hedges et al.

the blue marlin. Within istiophorids. 5. On the other hand. the blue marlin had a relatively wide head. The primary difference between the two was in rostrum length (Fig. In summary. 5. white marlin and shortbill spearfish (Fig.3). 5. 5. having the most fusiform shape (Fig. Wahoo. sailfish and white marlin. and swordfish were the most similar in overall shape of the skull and lower jaw length. Overall lower jaw reduction in length had an opposite pattern to rostrum elongation and followed the order in which billfish species were clustered in PC2 (Fig.4). For billfishes the longer the rostrum the shorter the lower jaw. Blue marlin had the widest skull. the sailfish skull was notably narrower than that of the blue marlin. However for the most part. the second longest rostrum.3).3). a large CSA of A1&A2 muscles and the largest bite force. the shortbill spearfish had a relatively wide and long head. The skull of the shortbill spearfish did not show an abrupt decrease in width at any investigated region when compared to blue marlin. with the two extremes found in swordfish and the shortbill spearfish (Fig. the out-group.3). Changes within istiophorids Within istiophorids the most extreme variation was between blue marlin and shortbill spearfish being primarily driven by the length of the rostrum. as well as lower jaw and head shape. The reduced head height makes Xiphias profile depressed compared to blue marlin. sailfish and white marlin had a conserved skull morphology. the lowest bite force a small cross sectional area of the muscles and the longest lower jaw. where the sailfish skull was compressed. Variation in skull width was notable between sailfish and white marlin. The rostrum of the swordfish was dorsoventrally compressed and laterally expanded. 125 . 5.

Head dimensions including head length positioned wahoo and swordfish together. White marlin and blue marlin share similarities in rostrum length whereas white marlin and sailfish are more similar in overall head shape (Fig.80 were considered correlated and are therefore discussed. Clusters were well defined among species and no outliers or large overlaps among taxa were detected. Only regressions with r (Pearson correlations coefficient) values above 0. However both white marlin and sailfish were similar in overall shape.g. white marlin and sailfish.2). 5. Blue marlin. and lower jaw length (PC 2 = 9. where the only noticeable differences were in head width and jaw length. skull width and height was found between sailfish and white marlin. Rostrum length separated wahoo and shortbill spearfish from swordfish on the horizontal axis and clustered blue marlin.2. 126 . Principal components analysis Principal component analysis (PCA) showed most of the variation among species was driven by rostrum length (PC 1 = 83. white marlin and sailfish in-between. Since numerous linear measurements were taken (e.2). The lowest amount of variation in rostrum length. white marlin and sailfish seem to be the three species with smaller differences. 5. and blue marlin. Table 5. lower jaw length. Correlation assessment in raw and phylogenetically corrected variables Results from the regression and correlation analysis showed a subset of variables with significant slopes among all species.8 % of variability) and cranial changes such as head length. with shortbill spearfish in the upper range. In this case the white marlin had a wider head and reduced jaw length.4 %) (Fig. head width was taken in four different regions of the skull).

5. 5).5. as head width (HW) increased so did head length (r= 0. cross sectional area of both adductor muscles (A1+A2 and A3) (r=0. only the general patterns are listed here. Rostrum length (RL) increase was related to increases in A2 cross sectional area (r=0.84).82) (Fig. Others patterns however remained the same (both slopes present Fig. Fig. and the same appears to hold for head width and the relationship the adductor muscles. Perhaps key to their success.88). 127 . 5.83). However.82).88. 0.5) only one had a high r value.94).5). so did lower jaw length (r=0.80).5) A major number of this relationships were absent after correcting for phylogeny (blue slope is either absent or with low r. 5. Although several new patterns emerged from the phylogenetically corrected regressions (blue slope only Fig.85) and anterior bite force (r=0. rostrum length with CSA of A3. and lower jaw length and in-lever. When head width decreased anterior mechanical advantage increased (r=-0. with more details in Fig. rostrum length (r=0. and A3 cross sectional area (r=0. lower jaw width (r=0. is the evolution of the rostrum. 5. As such. As head height (HH) increased. head width and anterior bite force were not correlated after phylogeny was taken into account. 5. head width increased as head height increased (r=0.93). in lever distance (r=0.numerous correlation results (r) are reported. Discussion Changes between billfish rostra and the skull The billfishes represent a small but seemingly morphologically diverse group of fishes that has exploited the pelagic realm.5) such as head width with head length. Among all species (including the wahoo).93).85) (Fig.

1985. The morphological analysis indicated that the billfish skull showed interspecific variation in some key characters.a structure believed to play a role in defense. Chapter 2) and their overall weight has been shown to be lighter than istiophorids (Ovchinnikov. 2014). 1968. Atkins et al.3. contrary to the shortbill spearfish where the rostrum is almost absent. 2 and 3) may be facilitated by the reduced lateral head profile and the smooth transition from the rostrum to the head as demonstrated by the morphometric analysis. Although skull reduction could be a disadvantage with respect to other performance measures. 2014. the overall size and mass reduction may be beneficial in other aspects such as hydrodynamics. Fierstine et. 1958. variation was mostly driven by changes in rostrum length (83.4). 1985. 1997). Fierstine. when size is accounted for. 1970).. 1925).. The skull of swordfish is characterized by a low level of mineralization and ossification (Nakamura. This reduction in overall bone weight may compensate for having the largest rostrum of billfishes. 2007. its skull showed a large reduction in all dimensions and skeletal elements (De Metrio et al. Scott and Tibbo. Fig. This feeding behavior also inferred from rostrum mechanics (Chapter. 1997. Stillwell and Kohler. swordfish and sailfish have low drag coefficients (Ovchinnikov. PC1).. 5. As expected. 1970). With regards to overall body shape. While swordfish have the most elongated rostrum. 1997. This low profile may lead to an overall drag reduction during lateral 128 . with the two extremes found between the shortbill spearfish and the swordfish (Fig..8 % of variability. Lateral swiping of the rostrum has been suggested as the primary feeding mode in swordfish (Bigelow and Welsh. Shimose et al. 5. 1970. such as lower bite force (see below in performance implications). and feeding (Wisner. Ovchinnikov. al. Domenici et al. The depressed profile of the swordfish rostrum is better suited than the marlin rostrum to reduce drag during lateral head striking (Chapter 2). drag reduction..

the larger epaxialis muscles and vertebral modifications in istiophorids suggest enhanced dorsoventral movement of the head in this group (Gregory and Conrad.). 1990) is absent in swordfish.. areas of attachment of the epaxialis muscles implies this muscle may be smaller in swordfish than in istiophorids which have enlarged processes.. this relationship was not found in billfish. 1937) Possible trade-offs Trade-offs may exist between feeding and sensory organs when morphological space is limited in the skull (Barel. McHenry et al. Camp and Brainerd. Other morphological variables may enable lateral swiping behavior. Finally. 1983. et al. In hammerhead sharks eye volume decreased while cephalofoil width increased (Mara. 2014).striking as previously proposed for crocodilians (Busbey. In contrast. 1995. the reduction of the posterior processes on the epiotic and pterotic bones. The importance in conserving billfish eye size may 129 . as in some cichlids (Husley et al. 2001. Devaere. perhaps suggesting the size of this organ is under stabilizing selection. and a smaller epaxialis may result in more limited dorsoventral movement of the head in swordfish. since eye size appears to be conserved (Ovchinnikov. 2002).. 2006) and snakes (Alfaro. Comm. Epaxialis muscles are responsible of head elevation in fish (Carrol and Wainwright. even when cross-sectional area of the jaw adductor muscles changed among species (Chapter 4). 2006. However. pers. 1970). The large interlocking zygapophyses responsible for an increase in stiffness in blue marlin’s vertebral column (Hebrank et al. Especially in swordfish where a reduction in skull dimensions was found.. et al. 2011). 2010). suggesting this species may have greater lateral flexibility (Long.. eye size did not change. An increase in the adductor muscle size in catfishes results in limited space for eye size (Devaere. 2007). Husley et al. 2001).

Dewar et al. Accordingly the head widens in the region of the hyomandibula in the billfishes. as wider heads may accommodate larger muscles as found in Darwin finches and sharks (Herrel et al. This is indicated by several other features such as endothermy and the modified extrinsic eye muscle that generates heat in all billfishes (Block. as may be the case in billfishes (Schmitz and Wainwright. 2005. 2005).. Shared ecological constraints in nocturnal reef fish have led to restrictions in eye diversity. 2007). Even when head width increased with A3 CSA. this was not the case in billfishes..reflect the selective pressures associated with a pelagic lifestyle. larger eyes will enhance light reception facilitating their pelagic lifestyle (Davie. 1987. The fact that A3 was shown not to be a predictor of biting performance in this group may explain this result (Chapter 2). Overall changes in morphology and feeding performance implications Regression and correlation analyses showed an increase in head width at the level of the hyomandibula (HW2) with an increase in the CSA of the adductor muscle subdivision A3 (Fig.. the origin of the jaw adductor division A3(Chapter 2).. 1990) and the large ratio of cones to ganglion cells in the retina that increases sensitivity to low light (Fritsches et al. The concomitant increase in head width and CSA of the adductor muscles seems intuitive. 2011).. 1990. 1997). 5. 2006). 1986. However. Huber et al. It is expected that skull architecture will reflect mechanical demands to help withstand concomitant increased muscle force (Herrel et al. 2003). De Metrio and Palmieri. 2011). Being open water and deep- diving predators.5). the lack of relationship of this variables with bite force suggest that other factors 130 . Changes in head width related to increase in muscle cross sectional area are expected to have performance consequences as occurs in turtles and lizards (Herrel and O’Reilly. the large size of the optic lobes reaching 22% of the brain size (Davie.

5. these findings must be taken with care because phylogenetic correction with such low species diversity (N=6) can lead to spurious results (Bloomberg. 2004. Chapter 2) play an important role in this performance measure (Herrel et al. 2007). A smaller fraction of skull variability was driven by changes in skull length and height as well as lower jaw length (9. The shortbill spearfish has one of the lowest biting performances and AMA among istiophorids. Kammerer et al. (Chapter 4). As described in the warping analysis. such as in gar and needlefish. have been associated to fast jaw closure characterizing species that feed upon elusive prey (Porter and Motta. 2004). This resembles the case of clariid catfishes where flattening and miniaturization of the 131 . In addition. and usually fast..4 % of variability. and not any functional demands as investigated here. warping analysis). Shortbill spearfish had the relatively longest lower jaw among istiophorids. suggesting that the increase in head width and the CSA of A1+A2 are due to relatedness. the skull of swordfish is reduced in all dimensions compared to istiophorids.4). 2006). Fast jaw closure versus high bite force jaws represent conflicting demands. Results from PC2 suggest that jaw length and skull elongation separates the shortbill spearfish from the rest of the istiophorids (Fig. PCA2. (that are bite force predictors in this group. with most of the elements of the suspensorium being substantially smaller. kinematically efficient jaws cannot achieve high bite forces (Westneat. 2003). the relationship between increased head width and increased bite force and A1+A2 CSA was not significant when phylogeny was taken into account. Long jaws. muscle origin or insertion and/or other muscles such as A1+A2.. However. With the lack of a rostrum for pre-processing of prey nor high bite force the shortbill spearfish may benefit from a more speed efficient jaw as reflected in its low AMA to increase its predatory success.such as muscle architecture (pinnate or parallel fibered).

2007). Prey items of swordfish are often severed in two or more pieces before swallowing. the reduction in skull size appears to be more prominent in 132 . primarily head length and lower jaw length. 2007). This was also observed in swordfish where bite force is lower than in any other billfish (Chapter 4). this species is believed to have lower drag than the swordfish and to be one of the fastest fishes (Krasnoperov. 2013). this may not be the case in swordfish since the rostrum may have assumed this function by decoupling prey pre-processing from the oral jaws. white marlin and blue marlin) (Fig. the billfish skull was found to vary in rostrum length and head shape. Sagong et al. Reduction in skull robustness has been linked to a decrease in biting performance in squamates (Herrel et al.skull is common among anguilliform species (Devaere e al.. blue marlin is one of the largest billfish species with the stiffest and the most mineralized rostrum (Atkins et al.). Within the three istiophorids that clustered together (sailfish. 1968. Some concomitant changes were present among the variables investigated. Eduard Walker Pers. 1985. Chapter 2) and has the largest absolute bite force recorded among billfishes (Chapter 4). 2001. Consequently having the most robust head may be related to the production and transfer of high stresses due to high bite force. 1935. presumably by lateral strikes of the rostrum (Scott and Tibbo. On the contrary. 2014. Sailfish showed the most elongated skull and blue marlin showed the stoutest skull. Nakamura. In summary.. 5. Although low biting performance can reduce feeding efficiency as shown in lizards by increasing the processing time to break down prey (Herrel. 2005).. Comm. and the large moments inflicted by the movement of a highly mineralized rostrum during swiping. differences were mostly related to head elongation. The streamlined shape of the sailfish skull may be related to their overall hydrodynamics.4). for example. Having a slender body.

had amongst the lowest bite force (Chapter 4).species with the largest rostrum (swordfish). however some differences were present as sailfishes showed the most elongated skull. Overall changes in morphology within these billfishes were not linked to a global decrease in feeding performance.. modifications on the vertebral column and body profiles that may influence billfish hydrodynamics. In istiophorids. Interestingly sailfish has been suggested to have one of the lowest drag coefficients in billfishes (Ovchinnikov. Huber et al. 2006). Sailfish. which had a narrow skull. The posterior portion of the skull was marked by robust processes at the distal end of the epiotic and pterotic bones. 133 . Feeding behaviors within the billfishes appear to be enabled by morphological variation not only on the shape of the rostrum but also perhaps by differing morphologies of the skull. blue marlin had the largest head. while white marlin had wider heads. fusiform and narrow skull. since potential decreases in performance such as bite force may be overcome by alternative structures such as the rostrum. 1970) perhaps as a result in part of the elongated. which was the case in white marlin that had the largest relative bite force.. and the longest lower jaw was found in species with the shortest rostrum (shortbill spearfish). Wider heads may be related to increased bite force (Herrel et al. the largest adductor muscles and largest bite forces. 2005. The istiophorid skulls that were morphologically similar were white marlin and sailfish. which were greatly reduced in swordfish.

Blomberg S. Proc.J.2011..Neer Sc. R. 83-109. B. M. J. Barel. Collette. 169-189. 134 .. 27. Motta. sailfish and spearfishes. PNAS. M. B. Block. C. Currey. 190. A.J.C.. Parin. Garland T. Soc. J. R. Nat. S. 335-354. KS: Allen Press 1. News Physiol. 1 Lawrence. 124.V. A.L. (2012). Herp.R..1412372111.. Morph. McGowen.D. (2014). 208-213. Ives. doi: 10. and Goldschmidt. Anker. M. Soc. Icht. Barel. Zool. and Shahar. Mito. Testing for phylogenetic signal in comparative data: behavioral traits are more labile.P.A.439-577 502. Special publication No.2454. T. (1984). F. J. 717-745. Sci. Amer.1073/pnas.References Atkins. (1987) Billfish brain and eye heater: A new look at nonshivering heat production.B. Remodeling of anosteocytic bone. Hoogerhoud..N. Cole Sallan.. Am. P.E. Neth.D. C. B. and Friedman. J. B.C. (1986) Structure of the brain and eye heater tissue in marlins.. (1984). Heads or tails: staged diversification in vertebrate evolutionary radiations.. 244-254.N.A. (2003). Constructional 581 constraint and its ecomorphological implications.1098/rspb. Acta Morph.H.. Block. (1989). Evolution 57. G. L. doi/10. Witte.. Carothers. Habegger. 2. 34. Sexual selection and sexual dimorphism in some herbivorous lizards. R. C. Teleostei): with a discussion on the implications for phylogenetic and allometric form-interactions. Form-relations in the context of constructional morphology: the eye and suspensorium of lacustrine Cichlidae (Pisces. (1984): Beloniformes: development and relationships. N. Dean.

. doi. W.M. Devaere. Viblanc.M. Oceanogr. Asiatic. Adriaens. Fish. B. Luo. Proc.. Hoolihan. L. (1940). Mem. G. Musyl.Davie.A.. and Teugels. J. S. (1997)..L.1098/rspb.. Nasby-Lucas.. 39.W. Orbesen.. (2001). with a revised species description of Platyallabes tihoni (Poll. H. Heat-producing organ of the swordfish (Xiphias gladius): A modified eye muscle... Zool.... Verraes W. P..G. 260. S. J. Krause. Prince... Verraes. E. Pacific Marlins: Anatomy and Physiology.. 255..W. The ontogeny of bite-force performance in American alligator (Alligator mississippiensis).. The allegated pugnacity of the swordfish and the spearfishes as shown by their attacks on vessels..P. Laurs.J. R.. P.0444.G. 219- 241. (1990).. J. How sailfish use their bills to capture schooling prey. Wilson. Lappin. Ditrich. H. D. Movements and behaviours of swordfish in the Atlantic and Pacific Oceans examined using pop-up satellite archival tags. New Zealand Massey Univ. N.org/10. 215-31. Steffensen.... E. and Palmieri. Bengal Branch.D. Marras. Morph. K. R. G.M. 317-327. Domeier. J. and Krause. G. Hist. Soc. Couillaud. 89-96. 1873) (Teleostei: Siluriformes): are adaptations related to powerful biting? J. J. Foley. Press. 135 .E. Mcnaughton. C. Dewar. G.D. Snodgrass. Palmerston North. P. 1653-1673. M.K. Roy. E. R. S.H. S... Morphology and spatial constraints in a dorso-ventrally flattened skull. 1944).M. Soc. Nat. (2005). Zool. Devaere S. Brill. Roy. Erickson.. P. J. A. De Metrio. J.. 234.. (2014). 2.. Herbert-Read. 2. M.K. D. Adriaens D. Cranial morphology of the anguilliform clariid Channallabes apus (Günther.M. Teugels G.. (2003). Lond. (2011).A. Block. Kurvers. Sepulveda. E. Gudger. Domenici.S.2014. A. D. and Van Vliet. 235-250.

8. Huber.L. Lond. H. P. The evolution of cranial design and performance in squamates: consequences of skull-bone reduction on feeding behavior. and underlies morphological innovation in the jaws of belonoid fishes.354-364. (2011). Hulsey. (2007). EvoDevo. C. Ph. M.. 103. A. C and Meyer. J. Biol. Soc. D. Comp. 125.T. Evol.J. Evolution of bite force in Darwin’s finches: a key role for head width. 47.D.P.C.J. Feeding biomechanics and theoretical calculations of bite force in bull sharks (Carcharhinus leucas) during ontogeny. 18. Huber. A. Herrel. Mims. Phylogenies and the comparative method.Dissertation:University of South Florida. Linn. Motta. S. 235 p. V. (1985).N. J. Am. Ontogenetic scaling of bite force in lizards and turtles. Herrel. D. Physiol. (2014). J.. and Hendry. P. M. Integr.R. Podos. 1-15 136 . (2007). Meyers. Revisiting de Beer’s textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronicgrowth. Biol. Huber. (2012). Soc..R.. Habegger. Do constructional constraints influence cyprinid (Cyprinidae: Leuciscinae) craniofacial evolution? Biol.. J.107-117. Koppermann. C.Gunter. Hollingsworth Jr. 79. 136-146. Biochem. A.R. and Ross. (2006)..A. Herrel. A.M. M.C. J.669-675.D. Cranial biomechanics and feeding performance of sharks. R. Streelman. Do constructional constraints influence cichlid craniofacial diversification? Proc.. Dean. C. J. 5. Metzger K.. and O’Reilly. Zoology 115. A. Hulsey. Nat. Felsenstein.. Zool.D. 274. 31-42..F.K. 1867-1875. Schaerlaeken. (2005). (2006).

148-161. and Bottjer. K. (1973). Fresh. Hawaii. Xiphiidae and Xiphiorhynchidae).W. Marshall. H. Seto Mar. Fierstine. I. Use of rostral characters for identifying adult billfishes (Teleostei: Perciformes: Istiophoridae and Xiphiidae). Nakamura. I. Zool. N. Stroud. Synop. 54. H.A. Res.J. Part 2. Jablonski.J. Copeia 1996. Fritsches. An Atlantic Blue Marlin. Mar.F.A. E. impaled by two species of billfishes (Teleostei: Istiophoridae).. 4th Edition. Billfish Symposium. Contributed papers.. Biol. Nakamura. University of Chicago Press. Fishes of the world.L. Billfishes of the world. Proc. Warrant. 255-396. E. (2003). Sci. Nelson. A paleontological review of three billfish families (Istiophoridae. Curr. H. 61. 2nd Int. 1-65. (2005). Pages 11-19 in R. 28. J. Warm eyes provide superior vision in swordfishes. Evolutionary innovations. Bull. H. R. 55-58. Fierstine.. Brill. Kailua-Kona. D. (1983).L. (1990). Mar. ed. (1990). In: M. Systematics of the billfishes (Xiphiidae and Istiophoridae).L. Biol. 22. K. (1996). FAO Fish. (1985). Liem. D. 253- 288.S. 15. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. (2005). 495-499. The ecology of evolutionary innovations: The fossil record. 1988. Syst. (1997). August 1-5. Publ.. New York: John Wiley & Sons.J. vol. N. K.L. 137 .. Lab. and Voigt. Makaira nigricans. Planning the future of billfishes. 5.Fierstine. 425-441. Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Warrant.H. 333-341.. No.J. Fritsches. Nitecki.125. FAO Species Catalogue. ed.

Swordfish and billfishes in the Atlantic Ocean. (2010). NOAA NMFS TT 71-50011.. (2013). Jeon. Ph.J. 124. Wainwright. Shimose. W-P. 138 . K. S. novelties and homology. Prog. Price. Morph. T.V.H. J.D. 54.J. Hydrodynamic characteristics of the sailfish (Istiophorus platypterus) and swordfish (Xiphias gladius) in gliding postures at their cruise speeds. R. and Motta.The morphology of the cephalic lobes and anterior pectoral fins in six species of batoids. Yokawa.0081323.C.C. 420-422. Evolution 64. 3057- 3068.Mara. Olsson. H. W. Res.C. S. D. Kazancioglu. Ovchinnikov. Istioampax marlina. L. and Tachihara. Ecology and functional morphology. L. V. Schmitz. and Near. J. Evidence for the use of the bill by blue marlin (Makaira nigricans). 274. 1070-1083. (2007). Bellwood. Vertebrate head development: segmentation. (2011).. (1964).. K. (2010). PLoS ONE doi:10. (2005).. (1970). 3258-3268. Sci. R. Evolution of the hammerhead cephalofoil: shape change.R. and P.pone.J.1371/journal. space utilization and feeding biomechanics in hammerhead sharks (Sphyrnidae). F. P. T. P..145-163. Coral Reefs. E. Saito. during feeding. Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes. L. Trans.. University of South Florida. Revell. Ericsson. D. Biosc.R. Isr. K.. Wainwright. Ichtyol. Copeia 1964.. T. M.30. Spearing behavior in feeding in the black marlin. Functional innovation and morphological diversification in parrotfishes. Evolution 63. Collar. Talbot. and Cerny. Mulvany. Choi. (2009) Size-Correction and Principal Components for Interspecific Comparative Studies. (2013). Dissertation.. Sagong. 415-428. and Penrih.J. 468.

Integ.C. T.J.L. Ecology. 31.. Syst. (2012). L. Biol. 1001-1027.. Zool. (1991). P.S. Wainwright. 139 . Evolution of levers and linkages in the feeding mechanisms of fishes. Biol. Comp. The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. P.L. 69. W.A.A. Sparks.Wainwright. (1988). Lachnolaimus maximus (Labridae). J. K.C. M. 213. 61. Morphology and ecology: the functional basis of feeding constraints in Caribbean labrid fishes. Wainwright. Price.W. P. Lond. Ferry. Zool.C. Wainwright.. J. Ecomorphology: experimental functional anatomy for ecological problems. 680-693. P.C. (2004). Amer. and Near. Tang. 378-389. Biomechanical limits to ecological performance: mollusks crushing by the Caribbean hogfish. (1987). Smith.. 283-298. 635-645. Westneat.. S. 44.

solandri). List of 55 landmarks utilized in 3D analysis in five species of billfish and the wahoo (A. Landmark definition R1 Most distal portion of the rostrum R2 Lateral edge of the rostrum at 25% (left) R3 Lateral edge of the rostrum at 25% (right) R4 Lateral edge of the rostrum at 50% (left) R5 Laterall edge of the rostrum at 50% (right) R6 Lateral edge of the rostrum at 75% (left) R7 Lateral edge of the rostrum at 75% (right) R8 Base of the rostrum at the level of lateral ethmoid (left) R9 Base of the rostrum at the level of lateral ethmoid (right) R10 Dorsal portion of the rostrum at 25% R11 Dorsa portion of the rostrum at 50% R12 Dorsal portion of the rostrum at 75% R13 Ventral portion of the rostrum at 25% R14 Ventral portion of the rostrum at 50% Mx1 Most anterior end of the maxilla (within the skull) (left) Mx2 posterior end of MX (Left) Mx3 Most anterior end of the maxilla (within the skull) (right) Mx4 posterior end of MX (right) M1 Most distal point of the dentary bone M2 Mostt posteroventral point of the articular bone (left) M3 Most posteroventral point of the articular bone (right) J1 midsection of the condylar portion of the quadrate bone between the quadrate-articular jaw joint (left) J2 midsection of the condylar portion of the quadrate bone between the quadrate-articular jaw joint (right) H1 Most ventral end of hyomandibula (left) H2 Most posterodorsal point of the hyomandibula where articulates to the pterotic bone (left) H3 Most ventral end of hyomandibula (right) H4 Most posterodorsal point of the hyomandibula where articulates to the pterotic bone (right) H5 Mostt anterodorsal point of hyomandibula where articulates with sphenotic bone (left) H6 Most anterodorsal point of hyomandibula where articulates with sphenotic bone (right) H7 point of origin of the adductor mandibulae muscles on hyomandibulae (left) H8 point of origin of the adductor mandibulae muscles on hyomandibulae (right) Sc1 Most anterior point of the sclerotic bone (left) Sc2 Most dorsal point of the sclerotic bone (left) Sc3 Most posterior point of the sclerotic bone (left) Sc4 Mostventral point of the sclerotic bone (left) Sc5 Most anterior point of the sclerotic bone (right) Sc6 Most dorsal point of the sclerotic bone (right) Sc7 Most posterior point of the sclerotic bone (right) Sc8 Most ventral point of the sclerotic bone (right) O1 Point at 50% of the lateral ethmoid bone (left) O2 Point at 50% of distance between R8/S1 (left) O3 Point of the suspensorium in line with 01 (left) O4 Point on the mesopterygoid in line with O2 (left) O5 Point at 50% of the lateral ethmoid bone (right) O6 Point at 50% of distance between R9/S2 (right) O7 Point of the suspensorium in line with 05 (right) O8 Point on the mesopterygoid in line with O6 (right) S1 Posterior process on the sphenoid bone (left) S2 Posterior process on the sphenoid bone (left) P1 Distal end of the pterotic bone (left) P2 Distal end of the pterotic bone (right) E1 Distal end of epiotic bone (left) E2 Distal end of epiotic bone (right) Ex1 Distal end of the process of the exoccipital bone (left) Ex2 Distal end of the process of the exoccipital bone (right) 140 .1.Table 5.

01 98.00 0.36 93.05 99.08 99.47 PC 6 0.00 0.00 0.33 PC 10 0.00 0.26 99.03 83.65 PC 13 0.03 99.00 0.00 0.02 99.29 97.00 PC 22 0.77 83.00 100.97 PC 20 0.01 PC 8 0.00 0.00 0.09 99.00 0.80 PC 15 0.46 PC 5 0.00 0.Table 5.02 99.89 PC 17 0.07 99.04 96.46 PC 11 0.99 PC 21 0. Results from PCA.00 1.85 PC 16 0.75 PC 7 0.17 PC 4 0.00 3.73 PC 14 0. loadings and variance for five billfish species and wahoo (A.01 100.93 PC 18 0.29 98.2.77 PC 2 0.00 0.00 0.18 PC 9 0.13 99.03 99.00 0.15 99.00 0.00 0.11 99.05 99.57 PC 12 0.00 0. solandri) Cumulative Eigenvalues Variance (%) Variance (%) PC 1 0.13 PC 3 0.00 1.00 0.00 9.17 99.00 141 .95 PC 19 0.

1. Missing landmarks are homologous to the ones shown in the left side and are described in Table 5. 5. indica) representing all landmarks utilized in six species of fishes. 142 .Fig. Left lateral and dorso-ventral view of blue marlin (M.1.

shortbill spearfish: T. (2006). albidus. Outline figures were modified from artwork by Diane Peebles. nigricans. 5. Phylogenetic relationships among five billfishes species (blue marlin: M. and a non-billfish outgroup species (wahoo: A.Fig. and internode branch-lengths were based on known divergence times reported by Hedges et al.2. Tree topology was based on Santini and Sorenson (2013). white marlin: T. albicans. sailfish: I. angustrirostris. solandri). 143 . swordfish: X. gladius.

Lateral and dorsoventral view of the skulls of the six fish species investigated. white marlin (T. 5.3. albicans). Species where arranged in phylogenetic order. swordfish X. shortbill spearfish (T. sailfish (I. From top to bottom: blue marlin (M. angustrirostris). solandri).Fig. gladius) and a non-billfish outgroup species (wahoo: A. 144 . nigricans). albidus).

wahoo A. Vertical axes (PCA 2) shows variation among species in head shape. shortbill spearfish T. albicans . gladius as green triangles.green rhomboids. Species are color and shape coded.4.Fig . Horizontal axes (PCA 1) shows variation among species in rostrum length. solandri . Swordfish X. nigricans .light blue “x”.dark blue circles. 145 . mostly head length and lower jaw length.5. Principal component analysis of 55 3-Dimensional landmarks in five species of billfish and the wahoo (A. angustrirostris . albidus . white marlin T.red “+”. solandri). sailfish I. the larger symbol within each cluster denotes the position of the average shape for each species. blue marlin M.turquoise squares.

5. lower jaw width (LJW=M2-M3). Regression and correlation matrix of 17 linear variables obtained from five billfish species and the wahoo (A. SCH=Sc2-sc4). Only slopes that were significantly are presented. Upper diagonals are the Pearson correlations (r) between traits. AM2=CSA A3). HW4= O2- O6). 146 . however this relationship is significant only with raw (red line). as well as anterior mechanical advantage and in lever (AMA. eye size (SCL=Sc1-Sc3. anterior bite force (ABF). In this example. HW2= H7-H8.Fig. after correcting the data for phylogeny this relationship is not significant (blue line is missing). adductor muscle cross sectional area (AM1=CSA A1+A2. head length (HL=R1-Ex1). HH2= M2-H5). rostrum length (RL=R1-O1).5. solandri).84). lower jaw length (LJL=M1-M2). head height (HH1) increases with lower jaw length (LJl) and both variables showed a strong correlation (r=0. HW3=S1-S2. The main diagonal described the traits compared: head width at four different areas of the skull (HW1= distance between O1-O5. and lever arms. Reported correlations are marked in grey and can be identified by the example denoted by arrows. head height (HH1= M2-Ep1. IL). Lower diagonals are the regression fits from non- phylogenetically corrected regressions (red) and phylogenetically corrected regressions (blue).

Rostrum morphology varies widely among billfishes but perhaps the two major bauplans can be summarized by comparing istiophiorids (marlins. Ovchinnikov. its length and presence or absence of teeth (Nakamura. 2007.. Aleyev. 1958. 1997). Fierstine et. Major differentiations are based on the cross sectional area of the rostrum. Fierstine.. 1977.. 1985. In addition. 1996). characters that are usually used for species identification (Fierstine and Voigt. Chapter 2. more recent kinematic and dietary studies suggest feeding as the most plausible option (Shimose et al. However. functional and morphological standpoint. 1997. al. sailfish and spearfish) and xiphiids (swordfish). 2014) where feeding repertoires may be categorized as species-specific (Talbot 147 . Domenici et al. paying special attention to the morphological variation of this structure and its possible functional implications and its tentative role in feeding. 2014). Previous studies have hypothesized different roles for this structure ranging from hydrodynamics to defense (Wisner. 1970. In this research I investigated the role of the rostrum in billfishes from a mechanical. major morphological differences in the rostrum have been suggested to have functional implications during feeding (Domenici et al. perhaps due to the logistical challenges associated to the study of this group. 3). CHAPTER SIX GENERAL CONCLUSIONS The role of the rostrum in billfishes was for many decades controversial..

Fierstine. Shimose et al.. In addition. Owing the lack of high peaks stresses along its length. material and structural commonalities between blue marlin (Makaira nigricans) and swordfish (Xiphias gladius) rostra may explain how to build an efficient biological beam that can act as a weapon in multiple ways. Fierstine et al. The common increase in stiffness towards the distal part of the rostrum may be suggestive of a “natural reinforcement’ where the rostrum may hit the prey. Scott and Tibbo. 1988. McGowan. In contrast. 2014). the internal conformation of the rostrum was conserved between species where acellular bone. the swordfish rostrum appears suited to be a more specialized uniaxial weapon where the arrangement of its skeletal material is maximized for 148 . Results from the mechanical analyses in Chapter 2 and 3 support the hypothesis that the rostrum is suited and used for feeding.. the blue marlin rostrum is built like a short.and Penrith. cartilage and adipose tissue were the major components of the rostrum. For example it was established from mechanical experiments and FEA models (Chapter 2 and 3) that the rostrum is mechanically capable of withstanding continuous loading. 1997. Despite these morphological differences. 1968. indicating that the morphological differences between swordfish and blue marlin rostra have functional implications and that species-specific differences in prey striking behavior is mechanically plausible. 1997. et al. 2007). no particular area of the rostrum may be prone to failure suggesting that by different strategies both rostra are likely to be used for feeding. including axial loading (Chapter 3).. Considering the possible role of the rostrum during feeding. stiff spear able to withstand larger magnitudes and ranges of loading. 1964. Behavioral inferences have been recently made in beetles were the geometry of the horns associated to their material properties were responsible in explaining differential fighting behavior (McCullough.

Moreno et al. 2005).. was shown to be low in this group compared to other non-billfish species such as sharks (Chapter 4). For example. Although failure stresses were not quantified in this research it was clear that the swordfish rostrum was more likely to fail under limiting conditions since it showed larger stresses than blue marlin in most loading regimes (Chapter 2 and 3). however in the case of the shortbill spearfish other cranial changes may play an important role to grant it success as a top predator (Chapter 5). 2005.lateral bending resistance while decreasing drag (Chapter 2). One of the lowest bite forces was found in swordfish. When comparing structures under similar loading conditions such as the standardized comparisons in the FEA models. 2009). contrary to my expectations rostrum length was not a bite force predictor (Chapter 4) as the shortbill spearfish (Tetrapturus angustrirostris) showed also low absolute and relative bite forces (Chapter 4).. However. 2008). 1984) suggesting the rostrum may decouple most of the prey processing from the oral jaws not relying in high bite forces to process its prey. 2010. the ones with larger stress will be more likely to fail (Rayfield... 2009). 2004. bite force a performance measure linked to skull architecture (Herrel et al. Although it is expected that large predators may generate high bite forces due to their size (Huber et al.. other strategies such as sharp teeth and venom glands have been shown to prevail in some top predators such as the great barracuda and the komodo dragon taking over the need for high biting performance (Habegger et al. Fry et al. 149 . For most billfishes the rostrum seem to be the most feasible strategy to compensate for low bite forces. The hypothesized function of the rostrum to play a crucial role in feeding may have played an important part in shaping other variables associated to its function and structure. the species with the largest rostrum (Nakamura.

Nikol’skii. the morphological characterization of blue marlin’s skull seems to further support this.. 2014. Although skull reduction could lead to disadvantageous outcomes such as decreased feeding performance due to low bite forces (Herrel. 1961. Gregory and Conrad. in swordfish this may be compensated with a long rostrum. It was demonstrated that the swordfish rostrum profile is best suited to reduce drag during lateral head shaking. 2. Chapter. This idea was also tested at a “whole body level” that suggested that swordfish and sailfish have low drag coefficients (Ovchinnikov. the largest absolute bite forces. 2007). 2014. 1970). overall skull reduction could be beneficial from a hydrodynamic standpoint. In addition. Chapter 2). 1937. 3 and 4). the well-developed processes of the epiotic and pterotic bones found in istiophorids are 150 . In addition. The overall decrease in the swordfish skull profile compared to istiophorids may offer additional support the hypothesized hydrodynamic enhancement (Chapter 5). as shown in the hydrodynamic analysis performed in Chapter 2. the largest adductor cross sectional areas and the stiffest rostrum (Atkins et al. For example. width and lower jaw length) as shown in the PCA and warping analysis (Chapter 5). where motions may be allowed in multiple directions.. This variation was mostly noticeable between istiophorids and xiphiids and some of these aspects of this variability seem to reflect possible modifications that support previously inferred feeding behaviors. This variation relies in rostrum length and head shape (head length. The mechanical description on the rostrum of this species support a more versatile rostrum. Warping and PCA analysis showed swordfishes to have a substantial decrease in the dimensions of its skull. In addition the light weight and low mineralization found in swordfish bones may affect its hydrodynamics and compensate for such a large rostrum (Atkins et al. The skull in billfishes is highly variable (Nakamura. 1985). Contrary to these results the blue marlin had the largest skull.

1970. 4 and 5). With a short and relatively less stiff rostrum (Atkins et al. The pelagic lifestyle of this group has been one of the most likely explanations for the large eyes and thermogenic specializations that enhance vision in this group (Fritsches. eye size seemed to be conserved among all billfishes even when muscle cross sectional area changed (Ovchinnikov.. pre-processing prey in shortbill spearfish appears not to rely on the use of the rostrum or high bite forces (Chapter 4). 1984). On the contrary. this species showed the relatively longest lower jaw among billfishes (Chapter 5) and this could be indicative of a more speed efficient jaw (Westneat. Interestingly no trade offs were found between sensory organs and feeding muscles as observed in cichlid fishes (Barel et al. due to the relatedness of the 151 . 2003). Within istiophorids perhaps the most disparate species is the shortbill spearfish. since billfishes seem to overcome potential decreases in performance such as bite force with alternative structures such as the rostrum. Larger epaxialis insertion processes may be associated with larger muscles used in head elevation. 2004) as reflected in its low AMA granting a faster prey capture prey than other istiophorids. et al. 2014). 3. (Chapter 4). lengthening of the lower jaw. suggesting this trait may be under stabilizing selection. showing one of the lowest biting performances and AMA among istiophorids. Chapter 5). These processes are associated with the epaxialis muscles which are linked to cranial elevation in bony fishes (Camp and Brainerd. or by acquiring different feeding behaviors (Chapter 2.. 2014). However. a movement that may be less likely to be used in swordfishes compared to the isiophorids. vanished after the data was corrected for phylogeny (Chapter 5). Several patterns of variable correlation originally detected among billfishes. indicating these relationships may be a result of phylogenetic inertia.considerably large and robust in blue marlin. Overall changes in morphology are not indicative of a decrease in feeding performance..

1999). 2003). 1999). several authors suggest a billfish ancestor to have a relatively short upper and lower jaw (Nakamura. Johnson. that different billfish species may rely on the rostrum more often for prey processing than bite force. 1986. Although this research has not investigated the evolutionary pathway of this structure. phylogenetic correction must be taken with caution since an evolutionary approach performed had low diversity (N=6) and could lead to spurious results (Bloomberg. Subsequent lengthening of the upper jaw into a bill or rostrum through evolution has been hypothesized to facilitate feeding and respiration (Fierstine. since biting performance is considerable weak in this group and that overall skull morphology may facilitate species specific feeding behaviors. Fierstine. However. overall results from this work suggest the rostrum is mechanically capable of being used during feeding. 1983. 152 . The rostrum and associated changes in skull shape suggest the rostrum may play a crucial role in the feeding repertoire of billfishes.species. Although the ancestral condition of the rostrum is still under debate.

Shortfin Mako..L. Barel. 148-161. J. Steffensen. Zool.439-577 502.L. Krause. Fierstine. 117-121.... impaled by two species of billfishes (Teleostei: Istiophoridae). R.J. Fierstine. 61. Kurvers. Ives A.. Currey...A. South. Fierstine. J. Mar. Acad.. doi. Viblanc.D. M. Roy.. impaled by blue marlin.M.. 34. P.L. Motta. Wilson.References Aleyev. Garland T.P.H. Dean. H. (1997). Form-relations in the context of constructional morphology: the eye and suspensorium of lacustrine Cichlidae (Pisces. 153 . Marras. Evolution 57:717-745.org/10. Habegger. Teleostei): with a discussion on the implications for phylogenetic and allometric form-interactions. Sci. Remodeling of anosteocytic bone. The Hague. Herbert-Read.L. Junk. Atkins. A. R. J. P. Cailliet.1073/pnas.0444..D. (2003). Domenici. S. 495-499. Nekton. and Voigt.M.. (1977).L. G. and Neer. An Atlantic Blue Marlin.1098/rspb. A. 3.J. Y. (2014). Isurus oxyrinchus. G. C. Bull. Proc. Testing for phylogenetic signal in comparative data: behavioral traits are more labile..71-77. (2014). Bull. How sailfish use their bills to capture schooling prey. J.2014. J. E. Fierstine. Calif. H. Makaira nigricans (Teleostei: Istiophoridae).. doi/10. H. Soc. S. Makaira nigricans. P. A new shortbilled marlin of the genus l11akaira. Couillaud. S. H. Copeia 1996. and Krause. and Shahar. Use of rostral characters for identifying adult billfishes (Teleostei: Perciformes: Istiophoridae and Xiphiidae). M.L.M. Neth. (1984). (1997).1412372111. Blomberg S. (1996). Tertiary Research 19. (1999). from the Yorktown Formation (Early Pliocene). PNAS. USA.R. Sci. N.N. P.E. eastern North Carolina at Lee Creek Mine.

Can.. Mc Cullough. Ingle. Biomech. G. van Osch.M. (2009).G. and Deban. P. 82. Habegger.A. Differential development of the rostrum and mandible of the swordfish (Xiphias gladius) during ontogeny and its possible functional significance. E.J.R. FAO Species Catalogue. D.. C. Mar.J. Luz. T. E. (1986). Fry. 39. 496-503..L. 54. Glannakis.P. M..J. N. Synop. Moreno.. 5. (1983). and Norman..J. Scanlon. Krishnasamy. E.. Zool. (1985).E. 8969-8974.... Hodgson.L. Mar. FAO Fish.. K. A. J. Huber D. Mallefet. Feeding biomechanics in the great barracuda (Sphyraena barracuda) during ontogeny.Fritsches. (2014) Structural adaptations to diverse fighting styles in sexually selected weapons. No..C. Emlen.. Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Bull.F.. 20-28. M..R. Citron. S. C. S.. (2010). Fresh. B. 66. Wroe. Sci. W. D. McNaughtan. 154 . Johnson. Karas.A. 63-72. and Herrel. Marshall. J. Zool. S. H. J. (1988). Warrant..(2009). Martelli. Scheib.W. Claes.. Nakamura. PNAS. A central role for venom in predation by Varanus komodoensis (Komodo Dragon) and the extinct giant Varanus (Megalania) priscus. Res. 283. 1-65. Is extreme bite performance associated with extreme morphologies in sharks? Phys. D. I. J. 111. Billfishes of The World.L. B.D. H. P. D. W.J. Scombroid phylogeny: an alternative hypothesis. 255-396. Winter.125. J. J. Nakamura. 333-341. J. 14484-14488 McGowan... Lab. K. E. McHenry. Goldstein. Lond. K. Seto Mar.. 106. Kochva.. Publ.. Zool.. E. Motta.M. J.. 1-41. (2003). Systematics of the billfishes (Xiphiidae and Istiophoridae). K.. Kwok. Huber.. Teeuwisse. Clausen.. PNAS.J. Biol.. Tobalske. P. 28. vol. I. Ferrara.

Spearing behavior in feeding in the black marlin. Rayfield. E. in the Western North Atlantic. and Tibbo. T. Xiphias gladius. and Penrih. Rayfield. 60-70. and Tachihara. R. Anat.. Talbot. Proc.. (2007). 420-422. 12. B.C. Cranial mechanics and feeding in Tyrannosaurus rex. M. Res. Shimose. Bd. J. D. Food and feeding habits of swordfish. F.J. 736-746. 1451-1459. 271. Evidence for the use of the bill by blue marlin (Makaira nigricans). Istioampax marlina. Copeia 1964. J. Trans. (1970). 44.. (2008). K. Canada. Westneat. T. Integ. K. K. 903-972.. Swordfish and billfishes in the Atlantic Ocean. 378-389.. 212. Res. Seasonal occurrence and feeding habits of black marlin (Istiompax indica). E. Royal Soc. Cranial performance in the Komodo dragon (Varanus komodoensis) as revealed by high resolution 3-D finite element analysis. 55. 54. Yokawa. M.N. Wisner..H. McHenry. Cunningham. V. Res.J. S. around Yonaguni Island. K. (1958). E. Clausen. Shimose. Ovchinnikov.. P. D’Amore. (2004). southwestern Japan. Saito. Scott. Yokawa. W... Wroe. Ecology and functional morphology [trans. 90-94. S. 468. (1968).Moreno. J. Is the spear of istiophorid fishes used in feeding? Pac. Sci. Fish. from Russian by Isr. K. Comp. Saito.W. Ichthyol. C. M.. 25.V. (1964). Biol. (2008). Lond. Prog. Evolution of levers and linkages in the feeding mechanisms of fishes. and Tachihara. Ichtyol. during feeding. NOAA NMFS TT 71- 50011]. Sci.B. 155 . (2004).

APPENDICES 156 .

157 .Appendix A: IACUC Protocol approval.

Appendix B. Permission to utilize MATLAB scrip and photographs for this research 158 .

159 .