Biologically-Inspired Systems Hermann Ehrlich Biological Materials of Marine Origin Vertebrates Tai Lieu Chat Luong Biologically-Inspired Systems Volume 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 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 Library of Congress Control Number: 2013934350 © Springer Science+Business Media Dordrecht 2015 This work is subject to copyright All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher’s location, in its current version, and permission for use must always be obtained from Springer Permissions for use may be obtained through RightsLink at the Copyright Clearance Center Violations are liable to prosecution under the respective Copyright Law The use of general descriptive names, registered names, trademarks, service marks, etc in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made The publisher makes no warranty, express or implied, with respect to the material contained herein Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) 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 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 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 Biomaterials of Vertebrates Origin An Overview 3 4 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 References 421 Nishida K, Tateishi C, Tsuruta D et al (2012) Contact urticaria caused by a fish–derived elastin–containing cosmetic cream Contact Dermatitis 67:171–172 Nivison–Smith L, Rnjak J, Weiss AS (2010) Synthetic human elastin microfibers: stable cross– linked tropoelastin and cell interactive constructs for tissue engineering applications Acta Biomater 6(2):354–359 Nomura Y, Kitazume N (2002) Use of shark collagen for cell culture and zymography Biosci Biotechnol Biochem 66(12):2673–2676 Copyright © 2002 Taylor & Francis Nomura Y, Toki S, Ishii Y (2000a) Improvement of the material property of shark type I collagen by composing with pig type I collagen J Agric Food Chem 48(12):6332–6336 Nomura Y, Toki S, Ishii Y et al (2000b) The physicochemical property of shark type I collagen gel and membrane J Agric Food Chem 48(6):2028–2032 Pfeiler et al (2002) Reprinted from Pfeiler E, Toyoda H, Williams MD, Nieman RA (2002) Identification, structural analysis and function of hyaluronan in developing fish larvae (leptocephali) Comp Biochem Physiol B Biochem Mol Biol 132(2):443–451 Copyright (Year), with permission from Elsevier Pouliot R, Azhari R, Qanadilo HF et al (2004) Tissue engineering of fish skin: behavior of fish cells on poly(ethylene glycol terephthalate)/poly(butylene terephthalate) copolymers in relation to the composition of the polymer substrate as an initial step in constructing a robotic/living tissue hybrid Tissue Eng 10(1–2):7–21 Prestwich GD (2011) Hyaluronic acid–based clinical biomaterials derived for cell and molecule delivery in regenerative medicine J Control Release 155(2):193–199 Prieto S, Shkilnyy A, Rumplasch C et al (2011) Biomimetic calcium phosphate mineralization with multifunctional elastin–like recombinamers Biomacromolecules 12(5):1480–1486 Raabe et al (2010) With kind permission from Springer Science+Business Media: Raabe O, Reich C, Wenisch S et al (2010) Hydrolyzed fish collagen induced chondrogenic differentiation of equine adipose tissue-derived stromal cells Histochem Cell Biol 134(6):545–554 Copyright © 2010, Springer Sakai S, Kim WS, Lee IS et al (2003) Purification and characterization of dermatan sulfate from the skin of the eel, Anguilla japonica Carbohydr Res 338(3):263–269 Shiratsuchi E, Ura M, Nakaba M et al (2010) Elastin peptides prepared from piscine and mammalian elastic tissues inhibit collagen-induced platelet aggregation and stimulate migration and proliferation of human skin fibroblasts J Pept Sci 16:652–658 doi:10.1002/psc.1277 Copyright © 2010 European Peptide Society and John Wiley & Sons, Ltd Reprinted with permission Tingbø MG, Pedersen ME, Kolset SO et al (2012) Lumican is a major small leucine–rich proteoglycan (SLRP) in Atlantic cod (Gadus morhua L.) skeletal muscle Glycoconj J 29(1):13–23 Volpi N, Schiller J, Stern R et al (2009) Role, metabolism, chemical modifications and applications of hyaluronan Curr Med Chem 16(14):1718–1745 Copyright © 2009, Bentham Science Publisher Reprinted by permission of Eureka Science Ltd Waterhouse A, Wise SG, Ng MK, Weiss AS (2011) Elastin as a nonthrombogenic biomaterial Tissue Eng Part B Rev 17(2):93–99 The publisher for this copyrighted material is Mary Ann Liebert, Inc publishers Reprinted with permission Wise SG, Mithieux SM, Weiss AS (2009) Engineered tropoelastin and elastin–based biomaterials Adv Protein Chem Struct Biol 78:1–24 Yunoki S, Mori K, Suzuki T (2007) Novel elastic material from collagen for tissue engineering J Mater Sci Mater Med 18(7):1369–1375 Chapter 14 Epilogue My efforts in the present work were to show the structural and chemical diversity in biological materials derived from marine fish, reptiles, birds and mammals as well as their material properties The scientific history of the discovery of these materials spans the last 150 years, and our own recent results may stimulate other researchers to rise to new challenges In the interest of, my book is dedicated to biological materials isolated, observed, or described in marine vertebrate organisms selected by the author Rather than a comprehensive work, this book is intended to provide an overview of a few organisms that demonstrate the high potential of future discovery in this field In these concluding remarks, I want to focus the attention of readers on some open questions, as well as on additional topics of interest These include fish gills, amphibian skin and sucking disk of sharksuckers Fish Gills Unique biomaterials-containing structures not discussed in this work are fish gills The function of gills is well described in the paper by Campbell et al (2008) “A fish continuously pumps water through its mouth and over gill arches, using coordinated movements of the jaws and operculum (gill cover) for this ventilation (Fig 14.1) A swimming fish can simply open its mouth and let water flow past its gills Each gill arch has two rows of gill filaments, composed of flattened plates called lamellae Blood flowing through capillaries within the lamellae picks up oxygen from the water Notice that the counter current flow of water and blood maintains a concentration gradient down which O2 diffuses from the water into the blood over the entire length of a capillary,” Campbell et al (2008) Two parallel sheets of epithelia separated by a narrow space for blood circulation and for the exchange of respiratory gases are the main structural components of gill lamella (Olson 2002; Wilson and Laurent 2002; Evans et al 2005) Correspondingly, surface area is increased due to this specific lamellar structure Also, so called collagen columns (Hughes and Grimstone 1965; Bettex-Galland and Hughes 1973; Wright 1973), which presumably function to prevent ballooning of the lamellae, are of crucial importance (Fig 14.2) Normally, collagen columns are surrounded by © 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_14 423 424 14 Epilogue Fig 14.1 Schematic of the teleost fish gill (CAMPBELL, NEIL A.; REECE, JANE B., BIOLOGY, 8th, ©2008 Printed and Electronically reproduced by permission of Pearson Education, Inc., Upper Saddle River, New Jersey) See text for details Fig 14.2 Diagrams to show the structure of fish gills (a) Single gill arch with two rows of filaments Secondary lamellae are drawn on the upper surface of one filament Directions of water and blood flow are indicated (b) Longitudinal section of two filaments showing secondary lamellae projecting above and below each filament (c) A single secondary lamella to show blood flow between pillar cells (d) Section across a secondary lamella showing epithelial, basement membrane, and pillar cell flange layers separating blood from the water Pillar cells with fine filaments are shown, and a column connects the two basement membrane layers (Republished with permission of The Company of Biologists Ltd, from Bettex-Galland and Hughes 1973; permission conveyed through Copyright Clearance Center, Inc.) 14 Epilogue 425 plasma membranes composed of pillar cells The function of these endothelial cells is to isolate columns from the circulation (see for details Hughes and Grimstone 1965; Wright 1973; Olson 2002; Wilson and Laurent 2002; Evans et al 2005) Thus two parallel sheets of respiratory epithelium are connected due to pillar cells with spool-shaped, cylindrical morphology “Usually five to eight collagen columns are enfolded by the plasma membrane of a pillar cell In the peripheral cytoplasm, pillar cells have numerous myofilaments that run parallel to the collagen columns,” (Kato et al 2007; see also Bettex-Galland and Hughes 1973) Thus, in the case of fish gills we can observe very a unusual role for collagen in the form of columns that must be definitively investigated in the future Recently, visiting the Zoological Museum at Christian-Albrecht University in Kiel (Germany), I found a well prepared skeleton of whale shark (Fig 14.3) with amazing gill rakers Gill rakers attached to the branchial arches have been hypothesized to be a component of all filtration mechanisms in fish The functions of the whale shark’s gills are: – to filter plankton using sieves-like microstructured rakers; – to extracting oxygen from large volumes of seawater Fig 14.3 Gill rakers of whale shark are morphologically very similar to whale baleen (Image courtesy of Andre Ehrlich) 426 14 Epilogue However, my interest is based on the high structural similarity between these gill rackers and those of whale baleen Intriguingly, our first measurements on mechanical properties of both biological materials showed very similar results Now, we are starting experimental work to investigate the chemical composition of gill rackers from whale sharks It would be very surprising to obtain analytical results confirming the keratinous nature of these gill rackers, as sharks and whales are related to fish and mammals, respectively This challenging and exciting task stimulates our attempts to obtain new knowledge Amphibian Skin Desalination or other water purification by use of membranes are topics of much current interest The skin of amphibians seems to be the source of bioinspiration for this application Both phenomena, which player crucial role in amphibian evolution, like gas exchange and free water movement across skin are based on specific permeability of their skin “Amphibians generally have very high rates of water turnover unless, like fossorial forms, they exploit environmental situations where water fluxes across their highly permeable skins are low Many amphibians have remarkable tolerances to osmotic imbalances, and are able to rectify these rapidly when water becomes available,” (Shoemaker and Nagy 1977; see also Neill 1958) Salinity potentially influences the abundance and distribution of amphibians by imposing osmotic stress (Smith et al 2007) The issue of salinity effects on amphibian biology and ecology has recently drawn more attention, for at least two reasons (see for review Wu and Kam 2009): first, several studies have revealed that amphibians breed in brackish water more commonly than originally thought, and that they exhibit interesting physiological and ecological adjustments to increased salinity stress; second, amphibians are important indicator species for freshwater ecosystems that face increased salinization due to natural causes, or to anthropogenic ones such as salt pollution resulting from road de-icing salt runoff In contrast to amphibians, reptiles, due to their low skin permeability, uricotelism, and salt glands, are well adapted to remain in water Amphibians adapted to saline media store solutes and remain at least slightly hyperosmotic to their environment (see for review Schoemaker and Nagy 1977) As discussed by Natchev and co-authors: “Due to their highly vascularised and permeable skins, amphibians have a low capacity to handle increased salinity in the waters they inhabit Nevertheless, a few species are able to live in brackish and even hypersaline waters Reports on adult amphibians, as well as their tadpoles, living under saline conditions are numerous; but only a few amphibians can survive prolonged exposure to sea water Among anuran species, adaptations to elevated salinity differ considerably One ranid species – the crab eating frog, Fejervarya cancrivora (Gravenhorst 1829) – is considered to possess the highest salinity tolerance among amphibians In this species, 50 % of the larvae survived in up to 80 % sea water – equivalent to 0.5 %M Cl,” (Natchev et al 2011; see also Beebee 1985; Dunson 1977; Karraker 2007; Sillero and Ribeiro 2010; Spotila and Berman 1976; Wu and Kam 2009) 14 Epilogue 427 Aside from F cancrivora, only two other anurans, the bufonid Pseudepidalea viridis and the pipid Xenopus laevis, are capable of tolerating higher than brackish salinities (Balinsky et al 1972; Hillmann et al 2009) The Crab-eating Frog is broadly distributed in India and Asia including mangroves, marshes, coastal scrub, and disturbed forests where it can tolerate both brackish and sea water Phylogenetic analysis supported the monophyly of the Fejervarya species, and the genome organization of F cancrivora mitochondrial DNA differs from that of neobatrachian frogs and typical vertebrates (Ren et al 2009) “The exceptional ability of F cancrivora to survive in saline media is probably related to the exceptionally high rates of urea production exhibited in this species Experimentation with unfed amphibians may lead to underestimation of salinity tolerance, because these fasting animals must deaminate a significant fraction of their protein to produce and maintain high concentrations of urea,” (Schoemaker and Nagy 1977) As the most salt-tolerant of all frogs (Hillmann et al 2009) it has been found under laboratory conditions to tolerate salinities of up to 29 ppt (Gordon et al 1961) Adults of this species survive in high salinity by maintaining a hyperosmotic plasma that uses the increased concentrations of sodium, chloride, and urea (Gordon et al 1961; Schmidt-Nielsen and Lee 1962; Gordon and Tucker 1968) Thus, the plasma of Fejervarya species helps them to survive in salt aquatic niches by topping up the ionic concentration with non-ionic solubilised urea Adult frogs have a different, and rather more unusual, method of osmotic regulation Instead of being osmoregulators and maintaining an imbalance between the osmotic concentration of their internal fluids and that of the exterior, they are partial osmo-conformers Internal osmotic concentration is matched with that of the exterior, at least in a hyperosmotic medium This is brought about not by manipulating ion levels, but by ‘topping up’ the ionic concentration of the plasma with the nonionic solute urea CO(NH2)2 Other amphibia show slightly raised urea levels under conditions of water shortage, but employing high urea levels to maintain osmotic balance with the environment is a habit shared only with elasmobranch fish (sharks, skates and rays) (Gordon et al 1961) Urea is the standard nitrogenous excretory product of ordinary adult amphibia, and is normally voided at the earliest convenient opportunity Indeed, given the solubility of urea, it is not an easy substance for a largely aquatic animal to retain, and it is not understood how Rana cancrivora (Fejervarya raja) achieves this Not only is it soluble and difficult to retain, urea is toxic: the concentrations of urea that occur in the frog’s plasma at exterior salinities of 80 % sea water, should denature enzymes and affect the binding of oxygen by haemoglobin Somehow R cancrivora copes with these hazards (Hogarth 1999) The crab-eating frog remains somewhat hypertonic to the external medium, even in the most concentrated solutions that have been tested This situation is maintained by the formation of urine which is more dilute than the plasma Since the skin is permeable to water, the inevitable result is an osmotic inflow of water from the medium, and this inflow permits the formation of urine without any necessity for the frog to drink the external medium There may be several advantages in this situation (Schmidt-Nielsen and Lee 1962) One is that the gastro-intestinal tract is not loaded 428 14 Epilogue with an excessive intake of magnesium and sulphate, which constitute roughly onetenth of the salts in sea water Another advantage in the formation of dilute urine is that this urine, if retained in the bladder, can serve as a water reservoir Osmoregulation of the crab-eating frog in sea water resembles that of elasmobranchs, except in that there is no evidence of active tubular reabsorption of urea in the frog (Smith 1936) The phenomenon of salt water resistance observed for this animal is also very intriguing from biomaterial science point of view, especially because of the skin properties Recent studies on crab-eating frogs in Indonesia confirms suggestions that these saltwater amphibians possess special skin resistance to water loss that allows them to reduce desiccation during the critical period of acclimation from land to salt water aerials (Wygoda et al 2011) Note that semi-aquatic species typically exhibit no skin resistance to water loss In 2010 Wygoda and co-workers discovered crab-eating frogs on Hoga Island, Indonesia Here, some results as follow: “The discovery presented an ideal opportunity to investigate water conservation in perhaps the world’s most unique amphibian Using gravimetric wind tunnel methods, the frog’s ability to resist water loss across the skin was tested High resistance values are common for arboreal and desert fossorial frogs, which may have values up to 300 s*cm−1 However, semi-aquatic species, like the crab-eating frog, typically exhibit no skin resistance, so that water evaporates at rates equal to free water surface (i.e sec/cm) Surprisingly, it was found a skin resistance value of 0.27 with a standard error of ± 0.06 s*cm−1 While this value seems small, the relationship between vapour density, water loss, and skin resistance means that modest increases in resistance may dramatically reduce overall skin evaporation rates,” (Bennett et al 2011) The adaptive advantage of evaporative water loss reduction in F cancrivora may be related to its amphibious behaviour and the time course of the mechanism by which it develops the ability to survive in waters of high salinity Crab-eating Frogs often move between fresh water and saltwater habitats (Wells 2007), but their compensatory establishment of elevated plasma solute levels is not accomplished immediately upon entry into high salinity water Indeed, Dicker and Elliott (1970) found that freshwater-acclimated frogs placed in solutions of >270 mOsm initially lost water osmotically that they did not recover for several days Extrapolating results of Dicker and Elliott (1970) to full-strength seawater (ca 2,000 mOsm) shows that freshwater-acclimated frogs moving into the sea would initially lose water at a rate of about 41 mg cm−2 h−1 A 50-g frog in seawater would fare somewhat better, reaching the same dehydration level in ca h Clearly, initial ventures into the marine environment must be short-lived for these frogs, especially for smaller juveniles, and it is during time on land that reduced evaporative water loss would be most beneficial A low-magnitude cutaneous resistance, for example, could prolong survival time on land by several hours The same 2.35-g frog in air, with a cutaneous resistance of 0.27 s cm−1 and in the water-conserving posture, could increase its time out of water by 1.5 h over a frog with no cutaneous resistance The larger 50-g frog under similar conditions could in-crease time on land by nearly h Reduced evaporative water loss probably continues to provide an advantage to frogs even after they fully acclimate to marine conditions, in that they must regularly venture back onto 14 Epilogue 429 land to restore urea that is continuously lost to the sea faster than it can be generated metabolically (Gordon and Tucker 1968) The mechanism responsible for reduced evaporative water loss in F cancrivora is unknown The only mechanism known to provide for reduced evaporative water loss in frogs in a given environment other than through cranial co-ossification or cocoon formation (see for review Wygoda et al 2011) is by lipid secretion onto the skin surface from lipid glands or lipid-secreting mucous glands (reviewed by Lillywhite 2006) The histology of F cancrivora skin has been examined and was found to be unique among amphibians in having (in addition to mucous glands) two previously undescribed glands (vacuolated and mixed) and no granular glands (Seki et al 1995) Because Seki et al (1995) did not stain their skin samples for lipids, it is not known whether any of these gland types are lipid sources Further examination of F cancrivora skin might help elucidate the mechanism that provides this species with its low level of resistance to evaporative water loss Sucking Disk The fish species termed Echeneis naucrates and known as the sharksucker was originally described by Linnaeus in 1758 The genus name, Echeneis, is derived from the Greek ‘echein’ meaning to hold and ‘nays’ meaning ship; suckling fish, or remora (see for review Richards 2006) In ancient time, Greek sailors believed in mysterious magical powers of sharksuckers which could slow down or even stop their ships Transportation of one organism by another, phenomenon known as phoresy, is related to characteristic behavioural features of remoras, which usually can be observed on large fish species like swordfish or tuna, or even, in the case of small specimens, traveling in the mouths or gills of large manta rays, sailfish, and ocean sunfish After the young remoras are about cm long, the sucking disc became visible and is fully formed when the fish reaches about cm In adult forms, the sucking disc is well visible due to a series of paired, transversely oriented, “pectinated lamellae” which forms the most conspicuous structure on the surface of dorsoventrally flattened head The pair of pectinated lamellae together with the interneural ray and intercalary bone represent the skeleton of the sucking disc (Bonnell 1962) “The main part of each pectinated lamella is formed by bilateral extensions of the base of the fin spine just above its proximal tip, each of which develops a row of spinous projections, or spinules, along its posterior margin The number of rows and the number of spinules increase with size, and they become autogenous from the body of the lamellae,” (Britz and Johnson 2012) (Fig 14.4) The spino-occipital and anterior spinal nerves are responsible for innervation of the muscles and the skin of the disc that is originally belonged to the anterior region of the trunk (Houy 1910) “A series of lateral line nerve innervated sense organs at the rim of the disk’s suction cup are similar in structure to Meissner’s corpuscles in mammals, sensitive to touch, and play an important role during the attachment of the remora The remarkable behaviour of remoras to attach to large animals in the water has led to a similarly fascinating, but true, use of remoras for catching fish and turtles This is only possible because of the great force that is needed to dislodge a remora once it has attached” (Britz and Johnson 2012; see also Fulcher and Motta 2006) 430 14 Epilogue Fig 14.4 Sharksuckers (above) possess unique sucking discs (below) (Image courtesy of George Burgess) What about the mechanism of disc action? This is described by Fulcher and Motta (2006) as follow: “Disk muscles erect or depress the numerous paired laminae, or toothed plates, which bear two to four rows of posteriorly directed spinules The erect laminae create a sub-ambient chamber, allowing these fish to adhere to other fish and inanimate objects Resting sub-ambient suction pressure differentials were recorded, as were the greatest sub-ambient pressure differentials as the fish were pulled posteriorly to simulate drag induced by a swimming host The resting pressure differential averaged –0.5 kPa, with no significant difference between Plexiglas® and shark skin surfaces With a force applied to their caudal peduncle, the echeneids generated suction pressure differentials averaging –92.7 kPa within the disk cavity while attached to Plexiglas On shark skin, the use of spinules increased friction and reduced the maximum sub-ambient suction pressure differential to –46.6 kPa; considerably more force (17.4 N) was required to dislodge the echeneids from the shark skin than from the smooth Plexiglas (11.2 N),” (Fulcher and Motta 2006) Here, I absolutely agree with Fulcher and Motta that “future research should investigate the relationships between sub-ambient suction pressure differential, disk size, and host specificity, as well as the possibility of greater reliance on spinules in species that adhere to rough-scaled hosts Furthermore, future research should References 431 examine the anterior blind chamber and its purported role as a pneumatic pump, and extend our findings by investigating the relationship between drag and suction pressure differentials when remoras are exposed to water of varying velocities in flume chambers,” (Fulcher and Motta 2006) It would be also be highly useful to obtain knowledge about the nanostructural organization of the disc, and the molecular interrelations on this level This book covers many different fields, and I hope it provides reader with a current survey of biomimetic applications for a diverse range of marine vertebrates While certain subjects I have covered here obviously warrant a more in-depth review, I hope this work server to stimulate interest and further investigations into these diverse interdisciplinary topics References Balinsky JB, Dicker SE, Elliot AB (1972) The effect of long term adaptation to different levels of salinity on urea synthesis and tissue amino acid concentrations in Rana cancrivora Comp Physiol Biochem 43B:71–82 Beebee TJC (1985) Salt tolerance of Natterjack Toad (Bufo calamita) eggs and larvae from coastal and inland populations in Britain Herpetol J 1:14–16 Bennett W, Dabruzzi T, Wygoda M (2011) Saltwater frogs exhibit water conservation to exploit their environment Published on-line http://www.biodiversityscience.com/2011/04/27/ saltwater-frogs-water-conservation/ Accessed 15 May 2014 © 2014 Biodiversity Science All Rights Reserved Bettex-Galland M, Hughes GM (1973) Contractile filamentous material in the pillar cells of fish gills J Cell Sci 13:359–370 Bonnell B (1962) Structure of the sucker of Echeneis Nature 196:1114–1115 Britz R, Johnson GD (2012) Ontogeny and homology of the skeletal elements that form the sucking disc of remoras (Teleostei, Echeneoidei, Echeneidae) J Morphol 273:1353–1366 Copyright © 2012 Wiley Periodicals, Inc Reprinted with permission Campbell NA, Reece JB, Urry LA et al (2008) Circulation and gas exchange, Chapter 42 In: Biology, 8th edn Pearson Benjamin Cummings, San Francisco ©2008 Printed and Electronically reproduced by permission of Pearson Education, Inc., Upper Saddle River, NJ Dicker SE, Elliott AB (1970) Water uptake by the crab-eating frog Rana cancrivora, as affected by osmotic gradients and by neurohypophysial hormones J Physiol 207:119–132 Dunson WA (1977) Tolerance to high temperature and salinity by tadpoles of the Philippine frog Rana cancrivora Copeia 1977:375–378 Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste Physiol Rev 85:97–177 Fulcher BA, Motta PJ (2006) Suction disk performance of echeneid fishes Can J Zool 84:42–50 Copyright © 2008 Canadian Science Publishing or its licensors Reproduced with permission Gordon MS, Tucker VA (1968) Further observations on the physiology of salinity adaptation in the crab-eating frog (Rana cancrivora) J Exp Biol 49:185–193 Gordon MS, Schmidt-Nielsen K, Kelly HM (1961) Osmotic regulation in the crab-eating frog (Rana cancrivora) J Exp Biol 38(3):659–678 Hillmann SS, Withers PC, Drewes RC, Hillyard SD (2009) Ecological and environmental physiology of amphibians Oxford University Press, New York Hogarth PJ (1999) The biology of mangroves Oxford University Press, Oxford, 228 p 432 14 Epilogue Houy R (1910) Beiträge zur Kenntnis der Haftscheibe von Echeneis Zool Jb Anat Ontog Tiere 29(for 1909):101–138 Hughes GM, Grimstone AV (1965) The fine structure of the secondary lamellae of the gills of Gadus pollachius Q J Microsc Sci 106:343–353 Karraker N (2007) Are embryonic and larval green frogs (Rana clamitans) insensitive to road deicing salt? Herpetol Conserv Biol 2:35–41 Kato A, Nakamura K, Kudo H et al (2007) Characterization of the column and autocellular junctions that define the vasculature of gill lamellae J Histochem Cytochem 55(9):941–953 Copyright © 2007, The Histochemical Society Reprinted by Permission of SAGE Publications.) Lillywhite HB (2006) Water relations of tetrapod integument J Exp Biol 209:202–226 Natchev N, Tzankov N, Gemel R (2011) Green frog invasion in the Black Sea: habitat ecology of the Pelophylax esculentus complex (Anura, Amphibia) population in the region of Shablenska Тuzla lagoon in Bulgaria Herpetol Notes 4:347–351 Copyright © 2013, Societas Europaea Herpetologica Reprinted with permission Neill WT (1958) The occurrence of amphibians and reptiles in saltwater areas, and a bibliography Bull Mar Sci Gulf Caribb 8:1–9 Olson KR (2002) Vascular anatomy of the fish gill J Exp Zool 293:214–231 Ren Z, Zhu B, Ma E et al (2009) Complete nucleotide sequence and gene arrangement of the mitochondrial genome of the crab-eating frog Fejervarya cancrivora and evolutionary implications Gene 441:148–155 Richards WJ (2006) Echeneidae: Remoras In: Richards WJ (ed) Early stages of Atlantic fishes, vol 2, An identification guide for the Western Central North Atlantic Taylor & Francis, Boca Raton, pp 1433–1438 Schmidt-Nielsen K, Lee P (1962) Kidney function in the crab-eating frog (Rana cancrivora) J Exp Biol 39:167–177 Seki T, Kikuyama S, Yanaihara N (1995) Morphology of the skin glands of the crab-eating frog (Rana cancrivora) Zool Sci 12:523–626 Shoemaker V II, Nagy KA (1977) Reproduced with permission of Annual Review of Physiology: Shoemaker V II, Nagy KA (1977) Osmoregulation in amphibians and reptiles Annu Rev Physiol 39:449–471, by Annual Reviews http://www.annualreviews.org Sillero N, Ribeiro R (2010) Reproduction of Pelophylax perezi in brackish water in Porto (Portugal) Herpetol Notes 3:337–340 Smith HW (1936) The retention and physiological role of urea in the elasmobranchii Biol Rev 11:49–82 Smith MJ, Schreiber ESG, Scroggie MP et al (2007) Associations between anuran tadpoles and salinity in a landscape mosaic of wetlands impacted by secondary salinisation Freshw Biol 52:75–84 doi:10.1111/j.1365-2427.2006.01672.x Spotila JR, Berman EN (1976) Determination of skin resistance and the role of the skin in controlling water loss in amphibians and reptiles Comp Biochem Physiol Part A 55:407–411 Wells KD (2007) The ecology and behavior of amphibians University of Chicago Press, Chicago Wilson JM, Laurent P (2002) Fish gill morphology: inside out J Exp Zool 293:192–213 Wright DE (1973) The structure of the gills of the elasmobranch, Scyliorhinus canicula (L.) Z Zellforsch Mikrosk Anat 144:489–509 Wu CS, Kam Y-C (2009) Effects of salinity on the survival, growth, development, and metamorphosis of Fejervarya limnocharis tadpoles living in brackish water Zoolog Sci 26:476–482 Wygoda ML, Dabruzzi TF, Bennett WA (2011) Cutaneous resistance to evaporative water loss in the crab-eating frog (Fejervarya cancrivora) J Herpetol 45(4):417–420 Index A Acanthodii, 8, 9, 18–19, 110 Acellular bone, 10, 11, 92–94, 231 Acrodin, 217–219 Adameloid, 217 Anal fin, 13–15, 278, 279, 281, 286–288, 300, 307 Antarctic fish, 23, 142 Aragonite, 134–136, 138–140, 145, 147, 148 Arctic fish, 23, 142 Armor-based constructs, 237 Aspidin, 5, 92, 93, 226, 231 B Barbels, 9, 107, 108 Bills, or beaks, 43–44 Biocomposites, 50, 91–182, 215, 222, 231, 245, 353, 411, 418 Biohalite, 165–166 Biologically controlled mineralization (BCM), 155 Biologically induced mineralization (BIM), 155 Biomagnetite, 153–158 Biomaterials, 3–49, 80, 104, 224, 263, 272, 321, 328, 334, 335, 351, 354, 371, 379, 390, 394, 405, 417, 418, 423 Biomechanics, 15, 16, 29, 46, 48, 76–79, 97, 121, 127, 133, 153, 226, 244–252, 285, 308, 362, 417 Biomedical applications, 69, 274, 335 Biomedicine, 84, 271, 272, 327, 328, 363, 371, 415–419 Biomimetic applications, 257–258, 431 Biomimetics, 15, 29, 50, 84, 104, 118, 237, 277, 291, 303, 308, 322, 410 Biomineralization, 32, 74, 75, 96, 106, 110, 116, 133, 137, 143, 144, 148, 150, 152, 156, 172–179, 218, 249, 250, 322, 393 Biopolymers, 50, 329, 347, 350, 354, 415 Biorobotics, 302–308 Biotechnology, 273 Bones, 5, 70, 91, 213, 241, 265, 292, 323, 343, 392, 419, 429 C Calcification, 73–75, 84, 141, 143, 149, 150, 172, 173, 179, 215, 293, 322, 334, 335, 393 Calcified structures, 135 Calcite, 134, 139, 140, 143, 145, 148, 151 Calcium hydroxyapatite crystals, 215 Calculi, 172–179, 181 Carcharhiniformes (Ground Sharks), 14, 81, 118 Cartilage, 3, 7–9, 11, 15, 19, 69–84, 92, 95, 97, 105, 160, 170, 327, 331, 343, 352–354, 364–366, 417 gelatin, 352–354 Cartilaginous endoskeleton, 9, 73 fishes, 9, 10, 77, 78, 82 Caudal fin, 16, 277–286, 300 Cetacean elastin, 368–371 Chalcedony, 179–181 Chondrichthyes, 8–11, 13, 73, 74, 84, 110, 116, 218, 303 Claspers, © Springer Science+Business Media Dordrecht 2015 H Ehrlich, Biological Materials of Marine Origin, Biologically-Inspired Systems 4, DOI 10.1007/978-94-007-5730-1 433 434 Class Acanthodii, 18–19 Amphibia, 4, 27–28 Chondrichthyes, 9–11, 13 Placodermi, 25–26 Class Aves (birds), 36–47 Class Cephalaspidomorphi (Petromyzontida), 7–8 Classification of marine vertebrates, 3–50 Class Myxini (Myxinoidea), 6–7 Class Osteichthyes (higher bony fishes), 19–21 Class Reptilia (reptiles), 28–36 Collagen, 5, 70, 92, 215, 244, 266, 283, 321, 345, 364, 382, 405, 415, 423 Collagenous composite material, 405 Composites, 213–231, 245, 294, 301, 330, 333, 347–349, 415 Coronoin, 217 Cosmine, 19, 25, 92, 117, 213, 220, 221, 223, 224 The Crocodilians (Order Crocodylia), 35 Ctenoid, 228–230 D Dentine, 4–6, 9, 10, 17, 18, 24, 25, 93, 104–107, 110, 111, 114–118, 121, 124, 125, 129, 131–133, 215–224, 231, 323, 324 Dentine-based composite, 218–221 Dermal bone, 8, 92, 94–95, 104, 107, 220, 241, 299 denticle, 9, 19, 106, 113, 230, 237 skeleton, 94, 114, 213, 220, 225, 226, 228, 241 Desmosine, 361, 365, 368 Dorsal fins, 12–15, 25, 278, 280, 286 Durodentine, 104, 106, 218, 219 E Earstones, 135 Egg-capsule proteins, 403–411 Egg-case, 10 Egg shells, 143–153 Egg tooth, 44–45 Elasmodine (isopedine), 219, 228 Elastin-like proteins, 70, 364–366, 415 Elastoidin, 292–297 Elastomers, Index Enamel, 4, 10, 19, 24, 104–107, 110–112, 114, 115, 117, 121–124, 128, 132, 133, 213, 215–224, 231, 250, 391 Enameloid, 5, 6, 104, 106, 107, 110–112, 114, 115, 117, 121, 133, 213, 215–218, 220, 221, 223, 227, 231 Endochondral bone, 73, 92, 95–96, 104, 292 Enteroliths, 172, 177 Eyes, 13, 14, 17–19, 24, 25, 29, 33, 38–39, 75, 161, 334 F Faecoliths, 172, 178 Films, 35, 151, 273, 302, 328, 331–334, 347–354, 378, 379, 382 Fin rays, 8, 107, 228, 229, 277, 279, 281, 282, 284–286, 291, 292, 296, 299, 302, 306, 307, 309 Fish armor, 238 elastin, 366–368 fins, 277–309 scales, 213–231, 237–259, 265, 269, 271–274, 325–327, 330, 335, 347, 416 skin, 245, 252, 256, 263–274, 323–325, 345, 346, 348, 351, 352, 415 wings, 289–291 Fish-like devices, 300–308 Flexible eggshell, 144, 147 Flying fish, 19, 21, 22, 278, 289–291, 307, 308 Folded teeth, 104, 115–116 G Ganoine, 19, 20, 219–221, 224, 228, 229, 249, 250 Gelatin based composite, 347, 348 Gelatin isolation, 355 Gels, 328, 329, 343, 345, 347, 349, 351, 353, 378 Gnathostomes, 4, 8–26, 71, 92, 94, 107, 364 Gular pouches, 45 H Hagfishes or Hyperotreti, Hagfish slime, 7, 379, 386–390, 417 Hard cartilage, 71, 84 Hemichordata, 69 Heterodontiformes (Bullhead sharks), 15 Hexanchiformes (Frilled and Cow sharks), 14 Hyaloine, 219, 220, 228, 230 Hypermineralized tooth plates, 104, 116–117 435 Index I Infraclass Chondrostei, 22 Infraclass Holostei, 22 Infraclass Teleostei, 22–23 Intermediate filaments, 377, 378, 380, 383–386, 394, 417, 418 Isodesmosine, 361 K Keratinization, 108, 380, 381 Keratinized teeth, 108–109 Keratin-like biological materials, 379, 417 L Lamniformes (Mackerel sharks), 15 Lamprey, 4, 7, 8, 70, 71, 73, 76, 81, 82, 108, 109, 134, 138, 306–307, 324, 364–366 Lampreys or Hyperoartii, Lizards (Suborder Sauria), 32 M Magnetosensitive neurons, 162 Magnetosome chain, 154–156 Map-and-Compass model, 157 Marine biopolymers, 415 collagens, 321–335, 415 elastin, 361–371, 418 gelatins, 343–355 keratins, 377–394 Vertebrate, 3, 50, 69–84, 96, 104, 106, 115, 120, 132, 133, 143–181, 289, 382, 418, 419, 431 Marine Mammals (Class Mammalia), 47–49 Marine structural proteins, 415–419 Materials, 3, 76, 97, 220, 237, 263, 277, 322, 344, 363, 378, 405, 415, 426 Materials engineering, 277–309 Medical aspect, 82–83 Membranes, 34, 38, 72, 81, 83, 91, 94, 105, 108, 134–136, 140, 143, 144, 147–152, 155, 156, 164–166, 170, 171, 218, 221, 244, 273, 292, 293, 300, 302, 307, 309, 324, 328, 333, 348, 349, 364, 378, 387, 405, 416, 424–426 Mesodentine, 9, 219, 226, 231 Microstructures, 29, 112, 131, 133, 144, 152, 153, 227, 242, 247, 257, 258, 425 Mineral-based composites, 213–231 Mineralization process, 101, 155 Mineralized cartilage, 69–84 tissues, 3, 91–181, 218, 219, 231, 249, 259 Mucocartilage, 71 Multiphase material, 103 N Narwhals, 48, 104, 122, 124–130 Narwhal tusk, 126–130 Nephroliths, 172, 176, 177 Non-mineralized cartilage, 69 O Order Anaspida, Batoidea, 15–16 Beloniformes, 21–22 Charadriiformes, 38 Chimaeriformes, 17–18 Cladoselachiformes, 12 Coelolepida, Cyclostomata, 6–8 Heterostraci, Osteostraci, Squamata, 32–36 Testudines, 30–32 Xenacanthiformes, 12–13 Order Procellariiformes (Tube-nosed Birds), 37 Order Selachii (typical sharks), 13–15 Order Sphenisciformes (Penguins), 37 Orectolobiformes (Carpet sharks), 15 Orientation and navigation processes, 157, 158, 162 Orthodentine, 110, 115, 121, 133, 218, 219, 226, 231 Otoconia, 133–143 Otoliths, 19, 133–143 P Pathological biomineralization, 172–179, 181 Pectoral fins, 12, 13, 16, 21, 22, 24, 92, 278, 279, 284–286, 289, 291, 297, 302–306, 308 Pelecaniformes order, 37 Pelvic fins, 8, 9, 13, 22, 78, 278, 279, 281, 288–289, 291 Perichondral bone, 9, 74, 92, 95 Petrodentine, 104, 106, 117, 121, 133, 219 Petromyzon marinus, 365 Pharyngeal denticles, 106, 110–112 Plicidentine, 104, 106, 115, 133, 219 436 Polyphenol, 405, 409–411 Polypterus, 21, 215, 216, 244, 249, 281, 282, 299 Practical applications, 141–142, 271, 335, 344, 394, 416 Prelomin, 218 Prismatic calcified cartilage, Pristiophoriformes (Sawsharks), 13 R Regeneration, 79, 80, 220, 221, 228, 272, 297–299, 329, 330, 333, 334, 349, 415, 419 Respiratory turbinates, 39 Rigid eggshell, 144 Robotics, 50, 118, 273, 274, 277–309 Rostral teeth, 109–110 Rostrum, 10, 13, 22, 29, 43, 77, 97, 98, 101, 104, 109, 110 S Salt glands, 31, 33–36, 39, 40, 164–171, 426 Saw or saw-snout, 10 Scaffolds, 80, 81, 271, 274, 328–330, 362, 379, 415, 416, 418 Sea snakes (Hydrophiinae), 33 Selfcleaning, 257–258 Semidentine, 219 Shagreen, 269–271 Shark teeth, 118–122, 217 Silica-based minerals, 179–181 Skeletal structures, 3, 15, 46 system, 94 Smart materials, 301–302, 363 Snakes (Suborder Serpentes, or Ophidia), 33 Soft cartilage, 71, 91 Soft eggshell, 144 Species richness and diversity of marine vertebrates, Spin-brush complex, 10, 11 Sponges, 31, 179, 181, 321, 322, 328, 331, 334, 344, 379, 382 Index Squaliformes (Dogfish), 14 Squatiniformes (Angelsharks), 13 Sting, 11 Structural proteins, 3, 70, 80, 321, 362, 365, 378, 380, 410, 415–419 Subclass Elasmobranchii, 11–12 Subclass Holocephali, 17 Subclass Sarcopterygii (lobe-finned fishes), 24–25 Superoleophobicity, 245, 256 Supraclass Agnatha (Jawless fishes), Supraclass Gnathostomata, Surface shape, 252–258, 286 T Teeth, 6, 78, 104, 213, 242, 380, 405 Tetrapoda, 26–49 Thelodont, 6, 226, 227 Tissue engineering, 79–82, 109, 263–274, 299, 300, 328, 330, 331, 354, 415–419 Tooth-like structures, 7, 91, 104–108, 225 U Uroliths, 172, 174, 176–179 Uropygial (preen) glands, 40 V Vasodentine, 219 Vaterite, 134, 140, 142, 143, 148, 150, 151 Vertebrate oral teeth, 114–132 Vestibular sensory apparatus, 133 W Walrus tusk, 48, 104, 130–132 Waterproof feathers, 40–41 Whale baleen, 390–394, 425, 426 Whale teeth, 104, 122–126 Wings and diving, 42–43 and flight, 41–42