Biological Materials of Marine Origin: Vertebrates

Biologically-Inspired Systems

Biological

Materials of

Marine Origin

Hermann Ehrlich

Vertebrates

Biologically-Inspired Systems

Volume 4

Series Editors

Prof. Dr. Stanislav N. Gorb, Christian Albrecht University of Kiel, Kiel, Germany

More information about this series at http://www.springer.com/series/8430

Hermann Ehrlich

Biological Materials

of Marine Origin

Vertebrates

ISSN 2211-0593 ISSN 2211-0607 (electronic)

ISBN 978-94-007-5729-5 ISBN 978-94-007-5730-1 (eBook)

DOI 10.1007/978-94-007-5730-1

Springer Dordrecht Heidelberg New York London

Library of Congress Control Number: 2013934350

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Hermann Ehrlich

Institute of Experimental Physics

TU Bergakademie Freiberg

Freiberg , Sachsen , Germany

v

Pref ace

The higher chordate subgroup includes all the vertebrates: fi sh, amphibians, reptiles,

birds, and mammals. All of them are found in marine environments and coastal

regions. Probably the animal that more closely defi nes human thoughts of life in the

sea is a fi sh. In fact, fi sh are an ancient group of animals whose origins date back

more than 500 million years. They are the most common and diverse group of ani￾mals with backbones in the ocean and in the world today.

These animals are the real goldmine for material scientists because of their aston￾ishing variety of shapes and sizes, as well as the diversity of biological materials that

compose their organs and structures. Herein are only a few examples. Fish possess

structures as barbels, claspers, denticles, scales, egg-cases, oral and pharyngeal teeth,

bones, otoliths, cartilage, swim bladders, sucking disks, epidermal brushes, fi ns, pel￾vic spines and girdle, gills and bony operculums, unculi and breeding tubercles, and

even wings in the case of fl ying fi sh. All of the listed structures are hierarchically

organised from nano to micro and macro scales. They possess very specifi c biopoly￾mers like collagens, elastoidines, elastins, keratins, and other cross-linked structural

macromolecules. Moreover, we can also fi nd such unique biocomposites of fi sh origin

with exotic names as hyaloine, ganoine, or cosmine. Did you know that terms as

enameloid, adameloid, coronoin, acrodin, and prelomin are related to fi sh scales? Or

the recent research detailing differences between orthodentine and osteodentine,

durodentine and vasodentine, plicidentine and mesodentine, semidentine and petro￾dentine, or elasmoidine, as forms of dentine in different fi sh species? If no, I hope you

are now intrigued by this book, which was announced in my fi rst monograph entitled

Biological Materials of Marine Origin: Invertebrates published by Springer in 2010.

In addition to fi sh, I also analyse biological materials from marine turtles, igua￾nas, snakes, and crocodiles as well as sea birds. Special attention is paid to whales

and dolphins, as representatives of marine mammals. In terms of species number,

marine mammals are a relatively small taxonomic group; yet given their biomass

and position in the food web, they represent an ecologically important part of marine

biodiversity. Furthermore they are of signifi cant conservation concern, with 23 % of

species currently threatened by extinction. Therefore, marine mammals often

feature prominently in marine conservation planning and protected area design.

vi

Both non-mineralized and biomineral-containing structures have been described

and discussed. Thus, bone, teeth, otoconia and otoliths, egg shells, biomagnetite,

and silica-based minerals are analyzed as biominerals. A separate chapter is dedi￾cated to pathological biomineralization. Furthermore, in this book, I take the liberty

to introduce the term “Biohalite” for the biomineralized excretion produced by the

salt glands of marine fi sh, reptiles, and birds. Further chapters are dedicated to

material design principles, tissue engineering, material engineering, and robotics.

Marine structural proteins are discussed from the biomedical point of view.

Altogether, the recent book consist of four parts: 14 chapters, including Introduction,

addendums, an epilogue, and addendums to each chapter including more than 2,000

references. Many of the photos are shown here for the fi rst time. I have also paid much

attention to the historic factors, as it is my opinion that the names of the discoverers of

unique biological structures should not be forgotten. As this is highly interdisciplinary

research, fully satisfying the curiosity of expert readers is diffi cult to do in this rather

short survey of a very broad fi eld. However, I hope it will provoke thought and inspire

further work in both applied and basic research areas.

There are so many institutions and individuals to whom I am indebted for the gift

or loan of material for study that to mention them all would add pages to this mono￾graph. It may be suffi cient to say that without their cooperation, this work could

hardly have been attempted. First of all, I am very grateful to Prof. Kurt Biedenkopf

and his wife Mrs. Ingrid Biedenkopf as well as to the German Research Foundation

(DFG, Project EH 394/3-1) for fi nancial support. I also thank Prof. Catherine Skinner,

Prof. Edmund Bäeuerlein, Prof. Victor Smetacek, Prof. Dan Morse, Prof. Peter

Fratzl, Prof. Matthias Epple, Prof. George Mayer, Prof. Christine Ortiz, Prof. Marcus

Buehler, Prof. Andrew Knoll, Prof. Adam Summers, Prof. Stanislav N. Gorb, Prof.

Arthur Veis, Prof. Gert Wörheide, Prof. Alexander Ereskovsky, Prof. Hartmut Worch,

and Prof. Dirk-Carl Meyer for their support and permanent interest in my research.

Especially I would like to thank Prof. Bernd Meyer and Dr. Andreas Handschuh for

the excellent scientifi c atmosphere at TU Bergakademie Freiberg where I enjoyed the

time to prepare this work. I am grateful to Prof. Joseph L. Kirschvink, Dr. Martin

T. Nweeia, and Dr. Regina Campbell-Malone for their helpful discussions of some

chapters, and to Dr. Vasilii V. Bazhenov, Marcin Wysokowski, Dr. Andrey

Bublichenko, Dr. Yuri Yakovlev, Alexey Rusakov, and Andre Ehrlich for their techni￾cal assistance. To Dr. Allison L. Stelling, I am thankful for taking excellent care of

manuscripts and proofs. To my parents, my wife, and my children, I am under deep

obligation for their patience and support during the years.

Freiberg, Germany Hermann Ehrlich

Preface

vii

Structure and function of biological systems as inspiration for technical developments

Throughout evolution, organisms have evolved an immense variety of materials,

structures, and systems. This book series deals with topics related to structure-func￾tion relationships in diverse biological systems and shows how knowledge from

biology can be used for technical developments (bio-inspiration, biomimetics).

ix

Contents

Part I Biomaterials of Vertebrates Origin. An Overview

1 Introduction ............................................................................................. 3

1.1 Species Richness and Diversity of Marine Vertebrates .................. 3

1.2 Part I: Biomaterials of Vertebrate Origin. An Overview ................ 4

1.2.1 Supraclass Agnatha (Jawless Fishes) ................................. 4

1.2.2 Gnathostomes ..................................................................... 8

1.2.3 Tetrapoda ............................................................................ 26

1.3 Conclusion...................................................................................... 49

References ................................................................................................. 50

Part II Biomineralization in Marine Vertebrates

2 Cartilage of Marine Vertebrates ............................................................ 69

2.1 From Non-mineralized to Mineralized Cartilage ........................... 69

2.1.1 Marine Cartilage: Biomechanics and

Material Properties ............................................................. 76

2.1.2 Marine Cartilage: Tissue Engineering ................................ 79

2.1.3 Shark Cartilage: Medical Aspect ........................................ 82

2.2 Conclusion...................................................................................... 84

References ................................................................................................. 84

3 Biocomposites and Mineralized Tissues ................................................ 91

3.1 Bone ............................................................................................... 91

3.1.1 Whale Bone: Size, Chemistry and Material

Properties............................................................................ 97

3.1.2 Whale Bone Hause ............................................................. 102

3.1.3 Conclusion.......................................................................... 103

3.2 Teeth ............................................................................................... 104

3.2.1 Tooth-Like Structures ......................................................... 106

3.2.2 Keratinized Teeth ............................................................... 108

x

3.2.3 Rostral Teeth ...................................................................... 109

3.2.4 Pharyngeal Denticles and Teeth ......................................... 110

3.2.5 Extra-oral and Extra-mandibular Teeth .............................. 113

3.2.6 Vertebrate Oral Teeth ......................................................... 114

3.2.7 Conclusion.......................................................................... 132

3.3 Otoconia and Otoliths .................................................................... 133

3.3.1 Chemistry and Biochemistry of Otoconia

and Otoliths ........................................................................ 137

3.3.2 Practical Applications of the Fish Otoliths......................... 141

3.3.3 Conclusion.......................................................................... 142

3.4 Egg Shells of Marine Vertebrates ................................................... 143

3.4.1 Eggshells of Marine Reptilia .............................................. 146

3.4.2 Egg Shells of Sea Birds ...................................................... 152

3.4.3 Conclusion.......................................................................... 153

3.5 Biomagnetite in Marine Vertebrates ............................................... 153

3.5.1 Magnetite in Marine Fish ................................................... 159

3.5.2 Magnetite in Marine Reptiles ............................................. 160

3.5.3 Magnetite in Sea Birds ....................................................... 161

3.5.4 Magnetite in Cetaceans ...................................................... 163

3.5.5 Conclusion.......................................................................... 164

3.6 Biohalite ......................................................................................... 164

3.6.1 Diversity and Origin of Salt Glands

in Marine Vertebrates ......................................................... 165

3.6.2 Salt Glands: From Anatomy to Cellular Level ................... 169

3.6.3 Conclusion.......................................................................... 171

3.7 Pathological Biomineralization in Marine Vertebrates .................. 172

3.7.1 Conclusion.......................................................................... 178

3.8 Silica-Based Minerals in Marine Vertebrates ................................. 179

3.8.1 Conclusion.......................................................................... 181

References ................................................................................................. 182

Part III Marine Fishes as Source of Unique Biocomposites

4 Fish Scales as Mineral-Based Composites ............................................ 213

4.1 Enamel and Enameloid .................................................................. 215

4.2 Dentine and Dentine-Based Composite ......................................... 218

4.3 Fish Scales, Scutes and Denticles: Diversity and Structure ........... 222

4.4 Conclusion...................................................................................... 231

References ................................................................................................. 231

5 Materials Design Principles of Fish Scales and Armor ....................... 237

5.1 Biomechanics of Fish Scales .......................................................... 244

5.2 Fish Swimming and the Surface Shape of Fish Scale .................... 252

5.2.1 Superoleophobicity of Fish Scale Surfaces ........................ 256

5.2.2 Selfcleaning of Fish Scales and

Biomimetic Applications .................................................... 257

Contents

xi

5.3 Conclusion...................................................................................... 259

References ................................................................................................. 259

6 Fish Skin: From Clothing to Tissue Engineering ................................. 263

6.1 Fish Skin Clothing and Leather...................................................... 264

6.2 Shagreen ......................................................................................... 269

6.3 Fish Scales and Skin as Scaffolds for Tissue Engineering ............. 271

6.4 Conclusion...................................................................................... 274

References ................................................................................................. 274

7 Fish Fins and Rays as Inspiration for Materials

Engineering and Robotics ...................................................................... 277

7.1 Fish Fins and Rays: Diversity, Structure and Function .................. 278

7.1.1 Fish Wings: Fins of Flying Fish ......................................... 289

7.2 Fish Fin Spines and Rays ............................................................... 291

7.3 Chemistry of Fish Fin: Elastoidin .................................................. 295

7.4 Fin Regeneration and Fin Cell Culture .......................................... 298

7.5 Robotic Fish-Like Devices ............................................................. 300

7.5.1 Fish and Designing of Smart Materials .............................. 301

7.5.2 Fish Biorobotics ................................................................. 302

7.6 Conclusion...................................................................................... 308

References ................................................................................................. 309

Part IV Marine Biopolymers of Vertebrate Origin

8 Marine Collagens .................................................................................... 321

8.1 Isolation and Properties of Fish Collagens..................................... 322

8.2 Fish Collagen as a Biomaterial ...................................................... 328

8.3 Conclusion...................................................................................... 335

References ................................................................................................. 336

9 Marine Gelatins ....................................................................................... 343

9.1 Fish Gelatin-Based Films ............................................................... 349

9.2 Shark Skin and Cartilage Gelatin ................................................... 352

9.3 Conclusion...................................................................................... 354

References ................................................................................................. 355

10 Marine Elastin ......................................................................................... 361

10.1 Elastin-Like Proteins in Lamprey .................................................. 364

10.2 Fish Elastin ..................................................................................... 366

10.3 Cetacean Elastin ............................................................................. 368

10.4 Conclusion...................................................................................... 371

References ................................................................................................. 371

Contents

xii

11 Marine Keratins ...................................................................................... 377

11.1 Intermediate Filaments ................................................................... 383

11.2 Hagfi sh Slime ................................................................................. 386

11.3 Whale Baleen ................................................................................. 390

11.4 Conclusion...................................................................................... 394

References ................................................................................................. 394

12 Egg-Capsule Proteins of Selachians ...................................................... 403

12.1 Collagen ......................................................................................... 405

12.2 Polyphenol-Containing Egg Capsule Proteins ............................... 409

12.3 Conclusion...................................................................................... 411

References ................................................................................................. 412

13 Marine Structural Proteins in Biomedicine

and Tissue Engineering........................................................................... 415

13.1 Conclusion...................................................................................... 418

References ................................................................................................. 420

14 Epilogue ................................................................................................... 423

References ................................................................................................. 431

Index ................................................................................................................. 433

Contents

Part I

Biomaterials of Vertebrates Origin.

An Overview

© Springer Science+Business Media Dordrecht 2015 3

H. Ehrlich, Biological Materials of Marine Origin, Biologically- Inspired Systems 4,

DOI 10.1007/978-94-007-5730-1_1

Chapter 1

Introduction

Abstract Marine vertebrates include fi sh, amphibians, reptiles, birds, and mammals.

The Part I describes the classifi cation of marine vertebrates. Included is information

about the broad diversity seen in specifi c biological materials. These materials

include mineralized tissues (cartilage, bones, teeth, dentin, egg shells), biominerals

(otoliths and otoconia), and skeletal structures (carapaces, sucking disks, spines,

scales, scutes, plates, denticles etc.). Elastomers (egg case) and structural proteins

(collagen, keratins) are also mentioned. Special attention is payed to the biomimetic

applications of biomaterials originating from marine vertebrates.

1.1 Species Richness and Diversity of Marine Vertebrates

The diversity of life forms on Earth is one of the most intriguing aspects for human

community. Therefore, knowing how many species inhabit the planet is one of the

most fundamental questions in modern science (Mora et al. 2011 ). The taxonomic

classifi cation of animal species into higher taxonomic groups (from genera to phyla)

follows a consistent pattern from which the total number of species in any

taxonomic group can be predicted. Assessment of this pattern for all kingdoms of

life on Earth predicts about 8.7 million species globally, of which ca. 2.2 million are

marine (Poore and Wilson 1993 ; Briggs and Shelgrove 1999 ; Bouchet 2006 ;

Appeltans et al. 2012 ). It suggests that some 86 % of the species on Earth, and 91 %

in aquatic niches, still await description (Mora et al. 2011 ).

Vertebrates, as important players in nearly all marine food webs, occupy all

marine habitats. The vertebrates in the ocean include fi sh, amphibians, reptiles,

birds, and mammals. The fi sh are the most successful in terms of numbers of

individuals as well as numbers of species (ca. 50 % of living vertebrates) (Berg

1940 ; Long 1995 ; Nelson 2006 ) and below, give an overview of classifi cations for

marine vertebrates. I include additional information about common and specifi c

biological materials like mineralized tissues, skeletal structures (spines, scales,

denticles), elastomers, structural proteins etc.

Among the most structurally complex organisms, marine vertebrates are classifi ed

under the Kingdom Animalia, Phylum Chordata and Subphylum Vertebrata. The

four main marine superclasses and classes, as well as one representative of marine

amphibians in Vertebrata, are discussed below.