Biological materials of marine origin vertebrates

Biologically-Inspired Systems

Hermann Ehrlich

Biological
Materials of
Marine Origin
Vertebrates

Tai Lieu Chat Luong


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 />

Hermann Ehrlich

Biological Materials
of Marine Origin
Vertebrates


Hermann Ehrlich
Institute of Experimental Physics
TU Bergakademie Freiberg

Freiberg, Sachsen, Germany

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
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Preface

The higher chordate subgroup includes all the vertebrates: fish, amphibians, reptiles,
birds, and mammals. All of them are found in marine environments and coastal
regions. Probably the animal that more closely defines human thoughts of life in the
sea is a fish. In fact, fish are an ancient group of animals whose origins date back
more than 500 million years. They are the most common and diverse group of animals with backbones in the ocean and in the world today.
These animals are the real goldmine for material scientists because of their astonishing 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, fins, pelvic spines and girdle, gills and bony operculums, unculi and breeding tubercles, and
even wings in the case of flying fish. All of the listed structures are hierarchically
organised from nano to micro and macro scales. They possess very specific biopolymers like collagens, elastoidines, elastins, keratins, and other cross-linked structural
macromolecules. Moreover, we can also find such unique biocomposites of fish origin
with exotic names as hyaloine, ganoine, or cosmine. Did you know that terms as
enameloid, adameloid, coronoin, acrodin, and prelomin are related to fish scales? Or
the recent research detailing differences between orthodentine and osteodentine,
durodentine and vasodentine, plicidentine and mesodentine, semidentine and petrodentine, or elasmoidine, as forms of dentine in different fish species? If no, I hope you
are now intrigued by this book, which was announced in my first monograph entitled
Biological Materials of Marine Origin: Invertebrates published by Springer in 2010.
In addition to fish, I also analyse biological materials from marine turtles, iguanas, 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 significant conservation concern, with 23 % of
species currently threatened by extinction. Therefore, marine mammals often
feature prominently in marine conservation planning and protected area design.
v

vi

Preface

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 dedicated 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 fish, 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 first 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 difficult to do in this rather
short survey of a very broad field. 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 monograph. It may be sufficient 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 financial 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 scientific 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 technical 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


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-function relationships in diverse biological systems and shows how knowledge from
biology can be used for technical developments (bio-inspiration, biomimetics).

vii



Contents

Part I
1

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

1.2 Part I: Biomaterials of Vertebrate Origin. An Overview ................
1.2.1 Supraclass Agnatha (Jawless Fishes) .................................
1.2.2 Gnathostomes .....................................................................
1.2.3 Tetrapoda ............................................................................
1.3 Conclusion......................................................................................
References .................................................................................................

Part II
2

3

Biomaterials of Vertebrates Origin. An Overview
3
3
4
4
8
26
49
50

Biomineralization in Marine Vertebrates

Cartilage of Marine Vertebrates ............................................................
2.1 From Non-mineralized to Mineralized Cartilage ...........................
2.1.1 Marine Cartilage: Biomechanics and
Material Properties .............................................................
2.1.2 Marine Cartilage: Tissue Engineering................................
2.1.3 Shark Cartilage: Medical Aspect........................................

2.2 Conclusion......................................................................................
References .................................................................................................

69
69

Biocomposites and Mineralized Tissues ................................................
3.1 Bone ...............................................................................................
3.1.1 Whale Bone: Size, Chemistry and Material
Properties............................................................................
3.1.2 Whale Bone Hause .............................................................
3.1.3 Conclusion..........................................................................
3.2 Teeth ...............................................................................................
3.2.1 Tooth-Like Structures .........................................................
3.2.2 Keratinized Teeth ...............................................................

91
91

76
79
82
84
84

97
102
103
104
106

108
ix


x

Contents

3.2.3 Rostral Teeth ......................................................................
3.2.4 Pharyngeal Denticles and Teeth .........................................
3.2.5 Extra-oral and Extra-mandibular Teeth ..............................
3.2.6 Vertebrate Oral Teeth .........................................................
3.2.7 Conclusion..........................................................................
3.3 Otoconia and Otoliths ....................................................................
3.3.1 Chemistry and Biochemistry of Otoconia
and Otoliths ........................................................................
3.3.2 Practical Applications of the Fish Otoliths.........................
3.3.3 Conclusion..........................................................................
3.4 Egg Shells of Marine Vertebrates ...................................................
3.4.1 Eggshells of Marine Reptilia..............................................
3.4.2 Egg Shells of Sea Birds ......................................................
3.4.3 Conclusion..........................................................................
3.5 Biomagnetite in Marine Vertebrates ...............................................
3.5.1 Magnetite in Marine Fish ...................................................
3.5.2 Magnetite in Marine Reptiles .............................................
3.5.3 Magnetite in Sea Birds .......................................................
3.5.4 Magnetite in Cetaceans ......................................................
3.5.5 Conclusion..........................................................................
3.6 Biohalite .........................................................................................
3.6.1 Diversity and Origin of Salt Glands

in Marine Vertebrates .........................................................
3.6.2 Salt Glands: From Anatomy to Cellular Level ...................
3.6.3 Conclusion..........................................................................
3.7 Pathological Biomineralization in Marine Vertebrates ..................
3.7.1 Conclusion..........................................................................
3.8 Silica-Based Minerals in Marine Vertebrates .................................
3.8.1 Conclusion..........................................................................
References .................................................................................................
Part III

109
110
113
114
132
133
137
141
142
143
146
152
153
153
159
160
161
163
164
164

165
169
171
172
178
179
181
182

Marine Fishes as Source of Unique Biocomposites

4

Fish Scales as Mineral-Based Composites ............................................
4.1 Enamel and Enameloid ..................................................................
4.2 Dentine and Dentine-Based Composite .........................................
4.3 Fish Scales, Scutes and Denticles: Diversity and Structure ...........
4.4 Conclusion......................................................................................
References .................................................................................................

213
215
218
222
231
231

5

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

5.1 Biomechanics of Fish Scales..........................................................
5.2 Fish Swimming and the Surface Shape of Fish Scale ....................
5.2.1 Superoleophobicity of Fish Scale Surfaces ........................
5.2.2 Selfcleaning of Fish Scales and
Biomimetic Applications....................................................

237
244
252
256
257


Contents

xi

5.3 Conclusion...................................................................................... 259
References ................................................................................................. 259
6

Fish Skin: From Clothing to Tissue Engineering .................................
6.1 Fish Skin Clothing and Leather......................................................
6.2 Shagreen .........................................................................................
6.3 Fish Scales and Skin as Scaffolds for Tissue Engineering .............
6.4 Conclusion......................................................................................
References .................................................................................................

263
264

269
271
274
274

7

Fish Fins and Rays as Inspiration for Materials
Engineering and Robotics ......................................................................
7.1 Fish Fins and Rays: Diversity, Structure and Function ..................
7.1.1 Fish Wings: Fins of Flying Fish .........................................
7.2 Fish Fin Spines and Rays ...............................................................
7.3 Chemistry of Fish Fin: Elastoidin ..................................................
7.4 Fin Regeneration and Fin Cell Culture ..........................................
7.5 Robotic Fish-Like Devices .............................................................
7.5.1 Fish and Designing of Smart Materials..............................
7.5.2 Fish Biorobotics .................................................................
7.6 Conclusion......................................................................................
References .................................................................................................

277
278
289
291
295
298
300
301
302
308

309

Part IV

Marine Biopolymers of Vertebrate Origin

8

Marine Collagens ....................................................................................
8.1 Isolation and Properties of Fish Collagens.....................................
8.2 Fish Collagen as a Biomaterial ......................................................
8.3 Conclusion......................................................................................
References .................................................................................................

321
322
328
335
336

9

Marine Gelatins.......................................................................................
9.1 Fish Gelatin-Based Films ...............................................................
9.2 Shark Skin and Cartilage Gelatin ...................................................
9.3 Conclusion......................................................................................
References .................................................................................................

343
349

352
354
355

10

Marine Elastin .........................................................................................
10.1 Elastin-Like Proteins in Lamprey ..................................................
10.2 Fish Elastin .....................................................................................
10.3 Cetacean Elastin .............................................................................
10.4 Conclusion......................................................................................
References .................................................................................................

361
364
366
368
371
371


xii

Contents

11

Marine Keratins ......................................................................................
11.1 Intermediate Filaments ...................................................................
11.2 Hagfish Slime .................................................................................

11.3 Whale Baleen .................................................................................
11.4 Conclusion......................................................................................
References .................................................................................................

377
383
386
390
394
394

12

Egg-Capsule Proteins of Selachians ......................................................
12.1 Collagen .........................................................................................
12.2 Polyphenol-Containing Egg Capsule Proteins ...............................
12.3 Conclusion......................................................................................
References .................................................................................................

403
405
409
411
412

13

Marine Structural Proteins in Biomedicine
and Tissue Engineering........................................................................... 415
13.1 Conclusion...................................................................................... 418

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

14

Epilogue ................................................................................................... 423
References ................................................................................................. 431

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


Part I

Biomaterials of Vertebrates Origin.
An Overview


Chapter 1

Introduction

Abstract Marine vertebrates include fish, amphibians, reptiles, birds, and mammals.
The Part I describes the classification of marine vertebrates. Included is information
about the broad diversity seen in specific 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
classification 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 fish, amphibians, reptiles,
birds, and mammals. The fish 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 classifications for
marine vertebrates. I include additional information about common and specific
biological materials like mineralized tissues, skeletal structures (spines, scales,
denticles), elastomers, structural proteins etc.
Among the most structurally complex organisms, marine vertebrates are classified
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.
© Springer Science+Business Media Dordrecht 2015
H. Ehrlich, Biological Materials of Marine Origin, Biologically-Inspired Systems 4,
DOI 10.1007/978-94-007-5730-1_1

3

4

1.2

1

Introduction

Part I: Biomaterials of Vertebrate Origin. An Overview

1.2.1

Supraclass Agnatha (Jawless Fishes)

Fossil evidence indicates that the group of agnathan (jawless fishes) species was
once highly successful and extremely varied. The oldest fossil remnants of agnathans
were found in Cambrian rocks. Only two groups, the lampreys and the hagfish,
with about 100 species in total, still survive today. The relationship between the
two clades, however, has not been resolved. There are two competing views: the
cyclostome (circular mouth) hypothesis and the vertebrate hypothesis. In the first,
hagfish together with lampreys form a monophyletic group, the Cyclostomata. In
the second, lampreys are sister to jawed fishes and all other jawed animals
(Gnathostomata) and together form the clade Vertebrata. The hagfishes, which lack
vertebrae, are the sister–group to the Vertebrata. The data in support of the cyclostome
hypothesis are mostly molecular, whereas those in support of the vertebrate hypothesis
are mostly morphological.
The problem of establishing homologies within and among the ingroups and
outgroups remains a challenge. It is of interest to note that Linnaeus (1758) classified

hagfishes in the class Vermes and the order Intestina (intestinal worms) and lampreys
in the class Amphibia and the order Nantes (swimming amphibians), erroneous
placements that nevertheless reflect their great divergence. Both, identifiable stomach
or any appendages have not been identified in all living and most extinct Agnatha.
These animals possess fertilization and development in external form without any
parental care. The Agnatha are cold blooded (ectothermic), and have a cartilaginous
skeleton. Extensively developed bony plates of many extinct agnathans are localized
directly under the skin. These served as protective armor and can be most often found
in the region of the skull. The extant agnathan species possess no bony plates (see
for review Xian–Guang et al. 2002; Janvier 2010; Renaud 2011).

1.2.1.1

Order Osteostraci

The Osteostraci are jawless and represent the sister taxon to jawed vertebrates.
Principally, they are integral to understanding the evolution of gnathostomes from a
jawless ancestor (Sansom 2009). The Osteostraci as a relatively compact group,
first appeared in the Late Silurian, flourished in the Early Devonian, but were
represented by only a few survivors by the Middle and Late Devonian (Robertson
1935). The surface of the exoskeleton of these animals was smooth, however
possess some small dorsal tubercles. Also the pores and grooves of the sensory
canal system and the related lateral lines were to detect. The thin layer of enamel,
underlain by a much thicker layer of dentine-like tissue, was located externally.
Together, the two formed the superficial layer. The dentine was perforated with
tubules that arose from a network of small vascular canals at the very top of the
middle layer (Denison 1947).


1.2 Part I: Biomaterials of Vertebrate Origin. An Overview

1.2.1.2

5

Order Anaspida

The anaspida were a now extinct order of fish-like vertebrates. In contrast to the
Osteostraci, their body, was less flattened and covered with dermal scales including
the head region. These animals possess hypocercal (tilting downwards) tail. Usually,
Anaspids were up to 15 cm in length. The Anaspids, which ranged from the Late
Silurian to the Late Devonian, included: Jaymoytius, Pharyngolepis, and Pterygolepis
(Allaby and Allaby 1999).

1.2.1.3

Order Heterostraci

The fossil group of heterostracans (Heterostraci) represents a large clade of the
Pteraspidomorphi. These armored, but jawless, vertebrates lived about 430–370
million years ago (from the Early Silurian to the Late Devonian). Their armored
head was generally fusiform and a tail fan-shaped. Both, the large dorsal and a large
ventral shield shields were formed by two plates. The exact morphological traits
with respect to scales are differing from one group of Heterostraci to another. For
example, such primitive forms as Lepidaspis, possess dorsal and ventral shields
which are composed of a mosaic of tiny scales.
From histological point of view, the scales observed in representatives of this
group, are distinct from other vertebrates. Their scales have dentine- and aspidinebased layers as well as an acellular bony tissue that is known to be unique to this
class (Halstead Tarlo 1963).
The so called “cancella” represents the honeycombed middle layer. In pteraspidomorphs, the unique biological material aspidin is present both in the attachment

of bone associated with the superficial dentine–enameloid tubercles, and in the
dermoskeleton which contains characteristic “spongy” and basal “lamellar” layers.
Aspidin is dominated by a collagenous fibrillar organic matrix and is acellular
(Donoghue and Sansom 2002).
There are about 300 species related to Heterostracans. They habituates were
sandy lagoons or deltas including marine environments with exception of some
fresh water species. They are known to occur in Europe, Siberia as well as in North
America. It is suggested that these animals were poor swimmers and probably
bottom-dwellers, and fed by scraping the bottom with their fan-shaped oral
plates that armed their lower lip. The representatives of Psammosteidae, developed
steer-like branchial plates and could grow up to 1.5 m in length and, however, most
heterostracans were relatively small (5–30 cm in total length). Their internal
anatomy is only known from the impressions of the internal organs on the internal
surface of the dermal armor because heterostracans have no calcified endoskeleton.
One may trace the impressions of two distinct vertical semicircular canals of the
labyrinth as well as of the gills, eyeballs, paired olfactory organ, and brain. Similar
to extant hagfish, their olfactory organs seem to have opened ventrally into a large,
median inhalant duct (see for review Halstead 1973; Janvier and Blieck 1979;
Janvier 1997a).


6

1.2.1.4

1

Introduction

Order Coelolepida

Thelodonts (from Greek: “nipple teeth”, formerly coelolepids) are an ensemble of
fossil jawless vertebrates, distinguished from other jawless vertebrate groups by the
structure of their minute scales-based exoskeleton (Wilson and Caldwell 1993).
These scales superficially resemble the placoid scales of sharks. Thelodonts lived in
shallow-water marine environments from the Lowermost Silurian (and possibly the
Late Ordovician) to the Late Devonian (430–370 million years ago) (Turner 1992).
It is suggested that some thelodonts migrated into fresh water, perhaps to spawn
(Van der Brugghen and Janvier 1993).
Probably, thelodonts were closely related and morphologically very similar to
fish of the taxa Heterostraci and Anaspida, differing mainly in their covering of
distinctive small, spiny scales. The small size and resilience of these scales makes
them the most common vertebrate fossil of their time.
The bony scales of the thelodont group were formed and shed throughout the
organisms’ lifetimes, and quickly separated after their death. Correspondingly, they
are the most abundant form of fossil as most resistant materials to the process of
fossilisation and thus most useful for analysis because of exceptional preservation
of internal details (Piepenbrink 1989). The scales contain an aspidine base and
comprise a non-growing “crown” composed of dentine, with a specifically ornamented
enameloid upper surface. The cell-free bone is the main element of its growing base,
including anchorage structures which fix it to the side of the fish.
It is established that five types of bone-growth, which may represent five natural
groupings within the thelodonts exist. Moreover, each of these scale morphs appears
to resemble the scales of more derived groupings of fish. Therefore, it can be hypothesized that thelodont groups may have been stem groups to succeeding clades of fish.
The taxa of thelodonts have traditionally been defined on the basis of histological
and morphological investigations of their scales. However, because a wide range
of scale morphologies can occur in the same individual, some recent studies on
articulated thelodonts show that scale morphology can be also misleading. On the
basis of their scale morphology and histology, thelodonts are currently classified
into following groups: Achanolepida, Loganiida, Turiniida, and Katoporida (see for

review Janvier 1997a).

1.2.1.5

Order Cyclostomata

Class Myxini (Myxinoidea)
Hagfishes or Hyperotreti. A taxon of ocean-dwelling fish, which are small and
jawless, as well as scavenging their food from both invertebrates and dead and
dying fish. They habituate in cold ocean waters of both hemispheres. Myxinikela
siroka is the only fossil hagfish, that remnants are localized in the Francis Creek
Shale of northeastern Illinois (Bardack 1991). Fragments of the head and jaws,
paired tentacles, internal organs were found within an iron carbonate (siderite)


1.2 Part I: Biomaterials of Vertebrate Origin. An Overview

7

concretion. Because the similarity to modern hagfishes is striking, it was suggested
that little evolutionary change in Myxini has been over the last 300 million years.
According to modern point of view (Kuratani and Ota 2008), these animals are
unique among living chordates. For example, they have a partial skull, but no vertebrae, and so they are not truly vertebrates. The skeleton lacks bone and is composed
of cartilage. Hagfish are almost blind, have no cerebrum or cerebellum, no jaws or
stomach, but three accessory hearts. They have four pairs of sensing tentacles
arranged around their mouth and also have well developed senses of touch and
smell. Interestingly, they can “sneeze” when their nostrils clog with their own slime.
Being jawless, a hagfish is equipped with two pairs of tooth-like structures, the
rasps, which are located on the top of a tongue-like projection. The pairs of rasps
pinch together after this tongue is pulled back into the hagfish’s mouth. This bite is

used in catching and eating marine invertebrates like polychaete worms, or to tear
into the flesh of dying and dead fish which have sunk to the muddy ocean bottom.
Principally, their metabolism is very slow, therefore hagfish may go for up to
7 months without eating any food. These vertebrates are slimy and capable of tying
their body into a knot. Furthermore, hagfish are known for producing large amounts
of slime when stressed (see also Sect. 11.2 in this work). The production of
the slime is believed to be some kind of defence mechanism against gill-breathing
predators. It was reported that the slime can reduce water flow over the gills of fish.
Slime thread skeins and mucin vesicles are two interacting components of hagfish
slime. Both are released from glands along the ventrolateral length of these primitive
vertebrates (see for review Downing et al. 1981; Lim et al. 2006).

Class Cephalaspidomorphi (Petromyzontida)
Lampreys or Hyperoartii are another group of primitive (Ruud 1954) and jawless
fishes. Non-parasitic species are able to eat only in their larval form, dying as adults
soon after reproducing. Parasitic species, however, latching onto the bodies of freshwater fish (Renaud and Economidis 2010). Lampreys have no jaws but possess an
annular cartilage that supports the supraoral and infraoral laminae. Their body is
naked and elongated. They possess seven branchial openings (or pores) on either
side of the body. The seven pairs of gill pouches are supported by a surrounding
branchial basket consisting of an elaborate network of fused cartilaginous elements.
Lamprey cartilage is unique to the group and contains hydrophobic protein lamprin
(Robson et al. 2000). The teeth on the oral disc and tongue-like piston of the adult
lamprey are made of keratin (Fig. 1.1). They possess a hollow core allowing for a
number of replacement teeth to occur one on top of the other. It has been estimated
that over the course of 2 years, an adult Sea Lamprey, Petromyzon marinus, may
replace its teeth about 30 times (Renaud 2011). The skeleton contains no bone, only
cartilage, although this cartilage may be calcified. The main axial support for the
body is the notochord, which is persistent throughout the life of the animal.
Rudimentary vertebral elements termed arcualia are arranged two per myomere on
either side along the dorsal nerve cord.

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Introduction

Fig. 1.1 Sea Lamprey teeth are located on the oral disc of lampreys (Photograph by Brian
W. Coad, image manipulation by Noel Alfonso. Canadian Museum of Nature www.briancoad.
com. Reprinted with permission.)

1.2.2

Gnathostomes

As reviewed by Janvier (1997b), the Gnathostomata, or gnathostomes, comprise the
majority of vertebrates from the Middle Devonian (about 380 million years ago) to
Recent. These animals differ morphologically from all other vertebrates by having
a vertically biting device, the jaws, which consist of and a variety of exoskeletal grasping, crushing, or shearing organs, and endoskeletal mandibular arch. Gnathostomes
possess the teeth, and jaw bones (Mallatt 1984). This group of recent vertebrates
include chimaeras, sharks, rays, ray-finned and lobe-finned fishes and terrestrial
vertebrates (see for review Schultze 2010).
The Chondrichthyes and Osteichthyes are two major clades of extant gnathostomes.
In addition, the Placodermi (Early Silurian-Late Devonian) and the Acanthodii
(Latest Ordovician or Earliest Silurian – Early Permian) are two extinct major
gnathostome clades. Outside of the taxa listed above, there may be other fossil
gnathostome groups, too.
The Chondrichthyes are characterized by the prismatic calcified cartilage, a
special type of hard tissue lining the cartilages of their endoskeleton. The pelvic

clasper is another chondrichthyan characteristic. This special copulatory organ is
derived from the posterior part of the pelvic fin (metapterygium). However, a pelvic
clasper may be present also in the fossil Placodermi. The Elasmobranchii and
the Holocephali represent two major extant clades of Chondrichthyans. Several
fossil clades like Cladoselachidae, Symmoriida, Xenacanthiformes, Iniopterygia,
Eugeneodontida may fall outside these two clades.
The Osteichthyes possess such specific characteristics in the endoskeleton as
endochondral (“spongy”) bone, dermal fin rays made up by modified, tile-shaped
scales (lepidotrichiae), and three pairs of tooth-bearing dermal bones lining the jaws
(premaxillary, maxillary and dentary). The Actinopterygii and the Sarcopterygii are
two major clades of the Osteichthyes.


1.2 Part I: Biomaterials of Vertebrate Origin. An Overview

9

The representatives of Placodermi possess a dermal armor consisting of head
armor and a thoracic armor. The thoracic armor is characterized by the foremost
dermal plates which form a complete “ring” around the body. It always includes at
least one median dorsal plate.
The Acanthodii differ from other clades by dermal spines inserted in front of all
fins but the caudal one. These animals also possess minute, growing scales with a
special onion-like structure, i.e. the crown consists of overlying dentine or
mesodentine-based layers.

1.2.2.1

Superclass Gnathostomata

Jawed fishes (99.7 % of all living fishes) and tetrapods are related to the Superclass
Gnathostomata. These vertebrates possess jaws and usually a set of paired appendages.
The superclass includes all the tetrapods: amphibians, reptiles, birds, and mammals.

Class Chondrichthyes
Cartilaginous fishes (about 1,000 species) possess primitive characters like
cartilaginous endoskeleton, single nostrils, and absence of the gas bladder. Modern
studies suggest that these vertebrates have a terminal position in the piscine tree
(Rasmussen and Arnason 1999a, b; Botella et al. 2009). They first appear in Upper
Silurian, and some fossil record starts in Lower Devonian. Representatives of this
class possess placoid scales, bony teeth of ectodermal and mesodermal origin in
jaws as well as teeth arranged in replacement whorls. Their endoskeleton is partially
covered with prismatically patterned perichondral bone, and their gill septum
extending to lamellar margin. The mosaic calcium carbonate-based granule pattern
is unique to these fishes. It is known that these mineralized structures on the outside
of the cartilage add strength. Both eggs and embryos of Chondrichthyans are large.
Similar to ray-finned fishes, representatives of this class have also large adults (from
20 cm and 15 g to 12 m and 12,000 kg).
From biological materials point of view, these fish possess numerous structures
with high biomimetic potential because of their unique physical, chemical and
material properties (Oeffner and Lauder 2012).
Below are listed some of these formations in alphabetical order:
Barbels – From morphological point of view, barbels are long conical paired dermal
lobes on the snouts of sharks. Their function is to locate prey. In contrast to most
sharks which have barbels associated with the nostrils, Sawsharks have barbels
in front of the nostrils.
Claspers – These paired copulatory organs are located on the pelvic fins of male
cartilaginous fishes. Animals use them for internal fertilization of eggs.
Dermal denticle – (or placoid scale) is an example of small tooth-like scale that is
unique to cartilaginous fish.

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Introduction

Egg-case – Flexible, horn-like protein-based envelope that surrounds the eggs of
cartilaginous fishes. In egg-laying species this is robust and necessary for protection of the egg. However, in live-bearers it is often membranous and soft, and
disintegrates while the fetuses are developing.
Rostrum – This cartilaginous structure is necessary to support the snout.
Saw or saw-snout – This elongated snout in sawsharks and sawfish possess
numerous side teeth formed from enlarged denticles. Usually is used to kill or
dig the prey (Fig. 1.2).
Spin-brush complex – unique spin-based structure described for Akmonistion
zangerli, one of the widely known representatives of Paleozoic chondrichthyans.
The spine of this fish (Fig. 1.3) consists of osteonal dentine surrounded by
acellular bone. It lacks any enamel-like surface tissue. The non-prismatic globular

Fig. 1.2 The saw- snout is formed from enlarged denticles. This is an ideal example of bioinspiration for engineers and materials scientists (Image courtesy of Mason Dean)


1.2 Part I: Biomaterials of Vertebrate Origin. An Overview

11

Fig. 1.3 Akmonistion zangerli possesses unique Spin-brush complex (Coates and Sequeira (2001),
reprinted by permission of Taylor & Francis Ltd, ( />
calcified cartilage is the main structural component of the brush and basal plate.

The peripheral regions of this specific matrix include a meshwork of crystal fibre
bundles. The leading edge and base of the brush are coated with a thin, acellular
bone layer of variable thickness (see for details Coates and Sequeira 2001).
Sting – The upper surfaces of the tails of most members of the stingray group
(Myliobatoidei) possess this large, flattened spine-like structure with several
side barbs.
Subclass Elasmobranchii
Two superorders, Batoidea (rays and their relatives) and Selachii (sharks), are typical
representatives of Elasmobranchs. These animals possess cylindrical or flattened
bodies covered by placoid scales. They have five to seven pairs of gill slits, their
upper jaw not fused to the cranium.


12

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Introduction

Batoidea include skates, electric rays, stingrays, guitarfish, and sawfish (see for
review Daniel 1922). They have five or six pairs of ventral gill slits and are characterized by a dorsoventrally flattened body. Their pectoral fins are fused to the head.
There are four orders and ca. 470 species of batoids.
Selachians include all species of sharks. These animals are characterized by a
fusiform body and five to seven pairs of lateral gill slits. Today, 8 orders and about
355 species of selachians are described. The diversity of elasmobranchs is well
described in the literature (see for review Thiel et al. 2009; Neumann 2006; Howe
and Springer 1993; Pollerspöck 2012).
Order Cladoselachiformes
Cladoselachidae (frilled sharks) is an extinct family of cartilaginous fish and among
the earliest predecessors of recent sharks. As the only members of the order

Cladoselachiformes, these animals were characterized by having an elongated body
with a spine in each of the two dorsal fins. According to Martin (2012), Cladoselache
specimens exhibited a combination of ancestral and derived characteristics. Their
jaw joints are weaker in comparison to modern-day sharks. However, they possess
very strong jaw-closing muscles. Its teeth were smooth-edged and multi-cusped,
making them ideal for grasping, but not tearing or chewing. It is suggested that
Cladoselache only seized prey by the tail and swallowed it whole. Unlike all
modern and most ancient sharks, frilled sharks swam the seas virtually naked.
Cladoselache’s skin seems to have been almost devoid of the tooth-like scales with
exception of small, multi-cusped structures along the edges of their fins, in the
mouth cavity, and around the eye.
Cladoselache’s scales serve as more than simple armor against injury. These
animals strengthen the skin to provide firmer attachments for their swimming
muscles. Their fin spines were odd, too.
Being short and blade-like, composed of a porous bony material, and located
some distance anterior to the origin of each dorsal fin, their spine fins were very
unusual. In contrast to other sharks with denser, more spike-like fin spines, that of
Cladoselache may have been lighter and sturdier. These structures may have reduced
swimming effort yet provided solid discouragement to would-be predators.
Order Xenacanthiformes
Xenacanthiforms are known from the Lower Carboniferous up to the Triassic
(Ginter 2004; Fischer et al. 2011). Their characteristics include articulated skeletons
and diplodont teeth, i.e. teeth with two lateral cusps evidently larger than the median
ones. For example, the recently discovered taxon Reginaselache morrisi is
identified by its teeth. These robust teeth possess multicristate cusps, as well as
prominent rounded coronal button, and a horseshoe-shaped labial boss. This shark
was about 1 m long, and probably fed on smaller paleoniscoid, invertebrates and
fish (Turner and Burrow 2011).

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13

There is also paleontological evidence that xenacanthids, predominantly adapted
to freshwater, have also lived in marine environments (Hampe and Ivanov 2007;
Ginter et al. 2010).
Order Selachii (Typical Sharks)
The order Selachii and the class Chondrichthyes (sometimes also called Selachii)
include different species of sharks, which majority can be traced back to around 100
million years ago (Martin 2006). These carnivorous animals use of food items ranging from plankton and fish to marine mammals and garbage. The young are born
alive as well as hatch within the female. About 350 living species of sharks are estimated today. Some of them are small like pygmy ribbontail catfish shark (less than
30 cm). Others are huge in size like the whale shark with up to 12 m length. These
magnificent creatures are able to live in every marine niche from the Arctic to the
tropics, and play a crucial role in keeping aquatic wildlife in balance (see for review
Compagno 2001). These animals keep prey populations in check and also function as
apex predators eating the weakest individuals (Stelbrink et al. 2010).
Living sharks are divided into eight suborders (see for review http://saltwaterlife.
co.uk/ws/sharkiologist/articles/shark-evolution-and-classification/):
1. “Squatiniformes (Angelsharks) have been around since the Triassic period (200–
250 mya). They are comprised of 19 species. They are found mainly in mud and
sand from cool temperate continental shelves, intertidal and continental slopes,
and in deeper water in the tropics. They are identified by their broad flattened
body, short snout, large pectoral and pelvic fins, two dorsal fins towards the
end of their tail, no anal fin and five gill slits. They look similar to rays superficially. However, the gill openings are on the sides of the head, not beneath as in
rays; and the large pectoral fins are clearly defined and separate from their
heads. They have large wide mouths at the front of their head perfectly designed
for ambushing their prey as they swim by the often sand covered shark. They are
ovoviviparous (they produce live young from eggs which hatch within the body)
with litter sizes between 1 and 25.

2. Pristiophoriformes (Sawsharks) first evolved during the Jurassic period (160–
200 mya). The suborder contains 9 species normally found on the continental
and insular shelves, in shallow water in temperate regions and deeper in the
tropics. They are probably the most distinct order amongst the shark groups, easily
identified by their flattened heads and long, flat, saw-like snout (the rostrum)
complete with barbells in front of the nostrils. Lateral and ventral teeth are used
to capture and kill prey, and possibly for courtship, competition and defence. The
lateral teeth erupt as the young are developing but lie flat along the rostrum
until after they are born. The eyes are located on the side of the head and they
have large spiracles, two dorsal fins and no anal fins. They are bottom dwelling
predators. Although data is lacking for most of the sawshark species it is known
that the Sixgill Sawshark Pliotrema warreni (the remaining eight species all have
five gill slits) is ovoviviparous and produces 5–7 pups per litter.