The Concept of Bone Tissue in Osteichthyes
Identifieur interne : 000359 ( Istex/Corpus ); précédent : 000358; suivant : 000360The Concept of Bone Tissue in Osteichthyes
Auteurs : Francois J. Meunier ; Ann HuysseuneSource :
- Netherlands Journal of Zoology [ 0028-2960 ] ; 1991.
Url:
DOI: 10.1163/156854291X00441
Links to Exploration step
ISTEX:6CA54C31B1AE225B8033DC8BCAE83B8CF1898482Le document en format XML
<record><TEI wicri:istexFullTextTei="biblStruct"><teiHeader><fileDesc><titleStmt><title>The Concept of Bone Tissue in Osteichthyes</title><author><name sortKey="Meunier, Francois J" sort="Meunier, Francois J" uniqKey="Meunier F" first="Francois J." last="Meunier">Francois J. Meunier</name></author><author><name sortKey="Huysseune, Ann" sort="Huysseune, Ann" uniqKey="Huysseune A" first="Ann" last="Huysseune">Ann Huysseune</name></author></titleStmt><publicationStmt><idno type="wicri:source">ISTEX</idno><idno type="RBID">ISTEX:6CA54C31B1AE225B8033DC8BCAE83B8CF1898482</idno><date when="1991" year="1991">1991</date><idno type="doi">10.1163/156854291X00441</idno><idno type="url">https://api.istex.fr/document/6CA54C31B1AE225B8033DC8BCAE83B8CF1898482/fulltext/pdf</idno><idno type="wicri:Area/Istex/Corpus">000359</idno><idno type="wicri:explorRef" wicri:stream="Istex" wicri:step="Corpus" wicri:corpus="ISTEX">000359</idno></publicationStmt><sourceDesc><biblStruct><analytic><title level="a">The Concept of Bone Tissue in Osteichthyes</title><author><name sortKey="Meunier, Francois J" sort="Meunier, Francois J" uniqKey="Meunier F" first="Francois J." last="Meunier">Francois J. Meunier</name></author><author><name sortKey="Huysseune, Ann" sort="Huysseune, Ann" uniqKey="Huysseune A" first="Ann" last="Huysseune">Ann Huysseune</name></author></analytic><monogr></monogr><series><title level="j">Netherlands Journal of Zoology</title><title level="j" type="abbrev">NJZ</title><idno type="ISSN">0028-2960</idno><idno type="eISSN">1568-542X</idno><imprint><publisher>BRILL</publisher><pubPlace>The Netherlands</pubPlace><date type="published" when="1991">1991</date><biblScope unit="volume">42</biblScope><biblScope unit="issue">2-3</biblScope><biblScope unit="page" from="445">445</biblScope><biblScope unit="page" to="458">458</biblScope></imprint><idno type="ISSN">0028-2960</idno></series><idno type="istex">6CA54C31B1AE225B8033DC8BCAE83B8CF1898482</idno><idno type="DOI">10.1163/156854291X00441</idno><idno type="href">1568542x_042_02-03_s022_text.pdf</idno></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">0028-2960</idno></seriesStmt></fileDesc><profileDesc><textClass></textClass><langUsage><language ident="en">en</language></langUsage></profileDesc></teiHeader></TEI><istex><corpusName>brill-journals</corpusName><keywords><teeft><json:string>chondroid</json:string><json:string>acellular</json:string><json:string>chondroid bone</json:string><json:string>meunier</json:string><json:string>isopedine</json:string><json:string>osteocyte</json:string><json:string>mineralization</json:string><json:string>huysseune</json:string><json:string>unmineralized</json:string><json:string>osteichthyes</json:string><json:string>acellular bone</json:string><json:string>teleostei</json:string><json:string>teleost</json:string><json:string>acellularization</json:string><json:string>basal</json:string><json:string>cellular bone</json:string><json:string>histological</json:string><json:string>basal plate</json:string><json:string>zool</json:string><json:string>articular</json:string><json:string>sire</json:string><json:string>matrix</json:string><json:string>osteichthyan</json:string><json:string>skeletal tissues</json:string><json:string>vertebrate</json:string><json:string>bone tissue</json:string><json:string>cellular</json:string><json:string>cement lines</json:string><json:string>elasmoid scales</json:string><json:string>other hand</json:string><json:string>cytoplasmic processes</json:string><json:string>bony tissues</json:string><json:string>huysseune verraes</json:string><json:string>mineralization front</json:string><json:string>evolutionary trends</json:string><json:string>mammalian bone</json:string><json:string>bony fishes</json:string><json:string>connective tissues</json:string><json:string>lower vertebrates</json:string><json:string>secondary bone</json:string><json:string>bone matrix</json:string><json:string>skeleton</json:string><json:string>cartilage</json:string><json:string>bone</json:string><json:string>skeletal tissue</json:string><json:string>acellularization process</json:string><json:string>spatial organization</json:string><json:string>entire skeleton</json:string><json:string>dorsal spiny</json:string><json:string>vascular canals</json:string><json:string>histological features</json:string><json:string>unmineralized isopedine</json:string><json:string>fibrous articular layer</json:string><json:string>medullary cavity</json:string><json:string>integumental skeleton</json:string><json:string>hard tissue</json:string><json:string>acellular scales</json:string><json:string>geraudie meunier</json:string><json:string>articular areas</json:string><json:string>fish bone</json:string><json:string>mature chondroid bone</json:string><json:string>upper pharyngeal jaws</json:string><json:string>various osteichthyan lineages</json:string><json:string>fine structure</json:string><json:string>articular process</json:string><json:string>poissons osseux</json:string><json:string>histological definition</json:string><json:string>pharyngeal jaws</json:string><json:string>neurocranial base</json:string><json:string>teleostei cichlidae</json:string><json:string>teleost fish</json:string><json:string>acta anat</json:string><json:string>early vertebrates</json:string><json:string>boca raton</json:string></teeft></keywords><author><json:item><name>Francois J. Meunier</name></json:item><json:item><name>Ann Huysseune</name></json:item></author><subject><json:item><lang><json:string>eng</json:string></lang><value>mineralization</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>bone</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>Osteichthyes</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>acellularization</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>chrondroid bone</value></json:item><json:item><lang><json:string>eng</json:string></lang><value>isopedine</value></json:item></subject><language><json:string>eng</json:string></language><originalGenre><json:string>research-article</json:string></originalGenre><qualityIndicators><score>4.428</score><pdfVersion>1.4</pdfVersion><pdfPageSize>426.96 x 672.72 pts</pdfPageSize><refBibsNative>false</refBibsNative><keywordCount>6</keywordCount><abstractCharCount>0</abstractCharCount><pdfWordCount>3916</pdfWordCount><pdfCharCount>28445</pdfCharCount><pdfPageCount>14</pdfPageCount><abstractWordCount>1</abstractWordCount></qualityIndicators><title>The Concept of Bone Tissue in Osteichthyes</title><genre><json:string>research-article</json:string></genre><host><volume>42</volume><pages><last>458</last><first>445</first></pages><issn><json:string>0028-2960</json:string></issn><issue>2-3</issue><genre><json:string>journal</json:string></genre><language><json:string>unknown</json:string></language><eissn><json:string>1568-542X</json:string></eissn><title>Netherlands Journal of Zoology</title></host><categories><wos></wos><scienceMetrix><json:string>natural sciences</json:string><json:string>biology</json:string><json:string>zoology</json:string></scienceMetrix></categories><publicationDate>1991</publicationDate><copyrightDate>1991</copyrightDate><doi><json:string>10.1163/156854291X00441</json:string></doi><id>6CA54C31B1AE225B8033DC8BCAE83B8CF1898482</id><score>0.027338427</score><fulltext><json:item><extension>pdf</extension><original>true</original><mimetype>application/pdf</mimetype><uri>https://api.istex.fr/document/6CA54C31B1AE225B8033DC8BCAE83B8CF1898482/fulltext/pdf</uri></json:item><json:item><extension>zip</extension><original>false</original><mimetype>application/zip</mimetype><uri>https://api.istex.fr/document/6CA54C31B1AE225B8033DC8BCAE83B8CF1898482/fulltext/zip</uri></json:item><json:item><extension>txt</extension><original>false</original><mimetype>text/plain</mimetype><uri>https://api.istex.fr/document/6CA54C31B1AE225B8033DC8BCAE83B8CF1898482/fulltext/txt</uri></json:item><istex:fulltextTEI uri="https://api.istex.fr/document/6CA54C31B1AE225B8033DC8BCAE83B8CF1898482/fulltext/tei"><teiHeader><fileDesc><titleStmt><title level="a">The Concept of Bone Tissue in Osteichthyes</title><respStmt><resp>Références bibliographiques récupérées via GROBID</resp><name resp="ISTEX-API">ISTEX-API (INIST-CNRS)</name></respStmt><respStmt><resp>Références bibliographiques récupérées via GROBID</resp><name resp="ISTEX-API">ISTEX-API (INIST-CNRS)</name></respStmt></titleStmt><publicationStmt><authority>ISTEX</authority><publisher>BRILL</publisher><pubPlace>The Netherlands</pubPlace><availability><p>© 1991 Koninklijke Brill NV, Leiden, The Netherlands</p></availability><date>1991</date></publicationStmt><sourceDesc><biblStruct type="inbook"><analytic><title level="a">The Concept of Bone Tissue in Osteichthyes</title><author xml:id="author-1"><persName><forename type="first">Francois J.</forename><surname>Meunier</surname></persName></author><author xml:id="author-2"><persName><forename type="first">Ann</forename><surname>Huysseune</surname></persName></author></analytic><monogr><title level="j">Netherlands Journal of Zoology</title><title level="j" type="abbrev">NJZ</title><idno type="pISSN">0028-2960</idno><idno type="eISSN">1568-542X</idno><imprint><publisher>BRILL</publisher><pubPlace>The Netherlands</pubPlace><date type="published" when="1991"></date><biblScope unit="volume">42</biblScope><biblScope unit="issue">2-3</biblScope><biblScope unit="page" from="445">445</biblScope><biblScope unit="page" to="458">458</biblScope></imprint></monogr><idno type="istex">6CA54C31B1AE225B8033DC8BCAE83B8CF1898482</idno><idno type="DOI">10.1163/156854291X00441</idno><idno type="href">1568542x_042_02-03_s022_text.pdf</idno></biblStruct></sourceDesc></fileDesc><profileDesc><creation><date>1991</date></creation><langUsage><language ident="en">en</language></langUsage><textClass><keywords scheme="keyword"><list><head>keywords</head><item><term>mineralization</term></item><item><term>bone</term></item><item><term>Osteichthyes</term></item><item><term>acellularization</term></item><item><term>chrondroid bone</term></item><item><term>isopedine</term></item></list></keywords></textClass></profileDesc><revisionDesc><change when="1991">Created</change><change when="1991">Published</change><change xml:id="refBibs-istex" who="#ISTEX-API" when="2016-10-10">References added</change><change xml:id="refBibs-istex" who="#ISTEX-API" when="2017-01-17">References added</change></revisionDesc></teiHeader></istex:fulltextTEI></fulltext><metadata><istex:metadataXml wicri:clean="corpus brill-journals not found" wicri:toSee="no header"><istex:xmlDeclaration>version="1.0" encoding="UTF-8"</istex:xmlDeclaration><istex:docType PUBLIC="-//NLM//DTD Journal Publishing DTD v2.3 20070202//EN" URI="http://dtd.nlm.nih.gov/publishing/2.3/journalpublishing.dtd" name="istex:docType"></istex:docType><istex:document><article article-type="research-article" dtd-version="2.3">
<front>
<journal-meta>
<journal-id journal-id-type="e-issn">1568542X</journal-id>
<journal-title>Netherlands Journal of Zoology</journal-title>
<abbrev-journal-title>NJZ</abbrev-journal-title>
<issn pub-type="ppub">0028-2960</issn>
<issn pub-type="epub">1568-542X</issn>
<publisher>
<publisher-name>BRILL</publisher-name>
<publisher-loc>The Netherlands</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.1163/156854291X00441</article-id>
<title-group>
<article-title>The Concept of Bone Tissue in Osteichthyes</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Meunier</surname>
<given-names>Francois J.</given-names>
</name>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Huysseune</surname>
<given-names>Ann</given-names>
</name>
</contrib>
</contrib-group>
<pub-date pub-type="epub">
<year>1991</year>
</pub-date>
<volume>42</volume>
<issue>2-3</issue>
<fpage>445</fpage>
<lpage>458</lpage>
<permissions>
<copyright-statement>© 1991 Koninklijke Brill NV, Leiden, The Netherlands</copyright-statement>
<copyright-year>1991</copyright-year>
<copyright-holder>Koninklijke Brill NV, Leiden, The Netherlands</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="1568542x_042_02-03_s022_text.pdf"></self-uri>
<kwd-group>
<kwd>mineralization</kwd>
<kwd>bone</kwd>
<kwd>Osteichthyes</kwd>
<kwd>acellularization</kwd>
<kwd>chrondroid bone</kwd>
<kwd>isopedine</kwd>
</kwd-group>
<custom-meta-wrap>
<custom-meta>
<meta-name>version</meta-name>
<meta-value>header</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<p>THE CONCEPT OF BONE TISSUE IN OSTEICHTHYES by FRANCOIS J. MEUNIER1 and ANN HUYSSEUNE2 (1 Laboratoire d'Ichtyologie, Muséum National d'Histoire Naturelle, 43 rue Cuvier, 75231 Paris Cédex 05, France, and Equipe de Recherche 'Formations Squelettiques, URA CNRS 1134, Université Paris 7, 2 place Jussieu, 75251 Paris Cédex 05, France. 2 Senior research assistant, Institut voor Dierkunde, Ledeganckstraat 35, B-9000 Gent, Belgium) ABSTRACT The purpose of this paper is to highlight the difficulties encountered when attempting to give a histological definition of bone tissue in Osteichthyes. Although the three basic components of bone tissue can be present (i.e. osteocytes, an organic matrix, and a mineral phase), it has long been known that bony tissues in Osteichthyes can lack trapped cells and/or mineral. This phenomenon has blurred the classical distinction between the generally adopted categories of connective tissues in a way that the osteichthyan skeleton should be described rather in terms of a continuum of structures. This paper illustrates this by discussing the evolutionary trends, within the Osteichthyes, of acellularization (i.e. the acquisition of acellular bone within the various osteichthyan lineages) and of loss of capacity of mineralization (e.g. in the case of isopedine of the basal plate of elasmoid scales). A further example of the difficulty of classifying skeletal tissues within bony fishes is provided by chondroid bone, a tissue with characteristics intermediate between cartilage and bone and found mostly in articular areas in the head of Teleostei. Each of the bone and bone-derived tissues of the aforementioned continuum represents the outcome of developmental and functional constraints, which appear to be more diverse in Osteichthyes than in Tetrapoda. KEY WORDS: Osteichthyes, bone, isopedine, chrondroid bone, acellularization, mineralization. INTRODUCTION The term 'bone' can denote different concepts (such as an anatomical organ, a tissue or even chemical components), depending on the level of integration of the skeletal structures 1. PETERSEN (1930) has defined four successive levels of integration of bone, and our aim is to consider the second- and third-order structures; they deal respectively with the fine anatomical and histological level of organization on the one hand, and with cells, extracellular matrix and minerals on the other hand (FRANCILLON-VIEILLOT et al., 1990). The two other levels of integra- tion (the first- and fourth-order structures, respectively describ- ing the anatomical and molecular arrangement of skeletal tissues) are 1 In this paper we have used the up-to-date nomenclature of FRANC ILLON-VIEILLOT et al. ( 1990); see also Ricc2,LES et al. ( 1991 ) and ZYLBERBERG et al. ( 1991 ).</p>
<p>446 irrelevant for the purpose of the present topic and will not be consid- ered here (but see FRANCILLON-VIEILLOT et al., 1990 and RICQLES et al., 1991 for more information). We will essentially discuss the prob- lems posed by osteichthyan bone when studying its histological organi- zation as revealed by the light microscope, and by transmission and scanning electron microscopy. The histological definition of bone as given in standard textbooks has been founded on studies of mammalian bone and more precisely of biomedical material (human, rat, dog ...) (see RICQLES et al., 1991). The very peculiar characteristics of human bone tissue (notably the Haversian system) have led to numerous generalizations, frequently resulting in many fundamental problems when looking at the skeleton of lower vertebrates. For example, the human Haversian organization of bone is very specialized, even amongst mammals (FRAN- CILLON-VIEILLOT et al., 1990), and is practically never encountered in lower vertebrates, especially bony fishes, although it is known in sev- eral dinosaurian reptiles (RICQLES, 1975). On the other hand, the majority of living fishes (and so perhaps of vertebrates) have bone without osteocytes (see below). So, an overview of bone tissues in vertebrates allows us to consider hard tissue as being clearly adaptive in most circumstances, rather than imposed by 'phylogenetic con- straints' more or less independent of functional demands (FRAN- CILLON-VIEILLOT et al., 1990). Bone typically is made up of three components: 1) bone cells: the osteogenic cells or osteoblasts, the trophic cells or osteocytes, and the clastic cells or osteoclasts; 2) extracellular organic material or organic matrix, i.e. the predominant network of collagenous fibres and the proteoglycans; 3) extracellular mineral material, essentially crystals of hydroxyapatite. Moreover, bone is frequently vascularized and is sub- mitted to resorption and reconstruction processes, e.l. remodelling (FRANCILLON-VIEILLOT et al., 1990; RICQLES et al., 1991). In the Osteichthyes, we can find bone with these typical basal components. However, the histological features of the bony tissues can vary according to the species and the bones considered, sometimes according to a particular part of the bone (MEUNIER, 1983; RICQLES et al., 1991). Since the middle of the 19th Century, studies on fish bone have shown that bone tissue displays a great variety of types, allowing authors to consider it as a wide continuum of structures. This is certainly the case when comparing e.g. bone with cartilage or with the so-called isopedine of the scale basal plate (basal plate composed of several superimposed plies of thick collagen fibrils organized in various plywood-like arrangements: twisted, orthogonal, ...; see MEUNIER,</p>
<p>447 1984, 1987). Indeed, the limits between the typical categories of skele- tal tissues are often vague with regard to their constitutive components and structural organization. The range of skeletal tissues, from cellular bone to nearly unmineralized acellular fibrous tissues, is an expression of the great adaptative trends of bone in various osteichthyan lineages. Two examples can illustrate these statements. The first concerns the double process of acellularization and lack of mineralization that affects several bone and bone-derived tissues (MEUNIER, 1984, 1987). The second one concerns so-called chondroid bone, which is fre- quently found in the Teleostei (HUYSSEUNE, 1989; BENJAMIN, 1990) and which is also known from the Tetrapoda (BERESFORD, 1981). THE ACELLULARIZATION PROCESS Osteocytes are the typical bone cells which progressively become entrapped in the bone matrix as the osteoblasts synthesize new bone. Osteocytes are star-shaFed, with cytoplasmic processes located within canaliculi in the bone matrix. In Osteichthyes the osteocytes show various features, especially related to the number and the length of the cytoplasmic processes (STEPHAN, 1900). For example, in Cyprinus carpio they are numerous, long and regularly distributed on the cell surface (fig. 1), whereas in Thunnidae they are scarce and inserted only in diametrically opposite positions (figs 2, 8). However, the initial work of WILLIAMSON (1851) and the fine studies of KOLLIKER (1859), con- firmed later by, amongst others, STEPHAN (1900), BLANC (1953) and Moss (1961a,b, 1963, 1965), have clearly shown that bone lacks osteocytes in numerous fishes (figs 3, 8). The histological features of such bone tissue are very similar to those of cellular bone, except that the osteocytes are missing. Such bone can show primary vascular bone as well as secondary bone, delimited from the former by cement lines, and a varying spatial organization of the collagenous network associated with remodelling processes (fig. 3). In some cases, as already mentioned by KOLLIKER (1859), STEPHAN (1900) or MEUNIER (1983), osteoblastic processes cross the bone matrix. Bone deprived of osteocytes, including bone with osteoblastic pro- cesses, is called acellular bone ('anosteocytic bone' of WEISS & WAT- ABE, 1979). The extensive studies of KOLLIKER (1859) and Moss (1961a,b, 1963, 1965), among others, have shown that the entire skeleton is made up either of cellular or of acellular bone. Within the Teleostei, cellular bone is found in the lower groups, whereas acellular bone has developed especially in advanced species. Nevertheless, there are two important exceptions: 1) the Protacanthopterygii (generally</p>
<p>448</p>
<p>449 Fig. 1. Longitudinal section (silver impregnation) of the dorsal spiny ray of Cyprinus carpio (Cyprinidae), showing typical star-shaped osteocytes with numerous cytoplasmic processes. (Bar = 50 pm.) Fig. 2. Longitudinal ground section (transmitted light) of a dorsal spiny ray of Katsuwonus pelamis (Thunnidae), showing spindle-shaped osteocytes; cytoplasmic processes are scarce. (Bar = 50 pm.) Fig. 3. Cross section (Masson's trichrome staining) in the supraoccipital of Trachurus trachurus (Carangidae), showing acellular bone. The latter has vascular canals (arrows) and consists of primary (pb) and secondary bone (sb) (specimen prepared by J. Laroche). (Bar = 100 pm.) Fig. 4. Detail of the mineralization front in a scale of Plagioscion squamosissimus (Sci- aenidae) showing coalescing polymorphic Mandl's corpuscles (arrowheads). (Bar = 100 pm.) Fig. 5. Cross ground section of a lateral line scale of Latimeria chalumnae (Coelacanthidae) showing the close contact (arrowheads) between mineralized secondary bone tissue and unmineralized isopedine. A) (top) Polarized light; B) (bottom) Microradiography. (from Meunier, 1980). (Bar = 250 pm.) Fig. 6. Chondroid bone on the autopalatine (left) and prevomer (right) of a nearly adult specimen of the cichlid Astatotilapia elegans, an acellular-boned fish. The chondroid bone is overlaid with a fibrous articular layer, consisting of fibroblasts (f) and osteoprogenitor cells (op). Osteoblast-like cells (ob) adjoin a narrow unmineralized zone (um). Below is the mineralized chondroid bone (CB). Note the gradual transition from the acellular tissue of the bone proper (AB) towards the cellular chondroid bone on the joint surface. Below the chondroid bone lies a medullary cavity (m). (Bar = 50 pm.) Fig. 7. Chondroid bone on the maxillla of a juvenile specimen of the cyprinid Cyprinus carpio, a cellular-boned fish. Note the chondrocytic appearance of the cells in the chondroid bone (CB). (Bar = 20 pm.) considered as relatively primitive fishes) have acellular bone, except the Salmonidae; 2) within the Acanthopterygii (the more evolved tele- osts), the Thunnidae have cellular bone. The presence of cellular bone in Thunnidae is generally considered the consequence of these ani- mals' high metabolic activity. All the living non-teleost fishes have cellular bone: Coelacanthidae, Dipnoi, Lepisosteidae, Amiidae, Polyp- teridae and Chondrostei. Nevertheless, this scheme is somewhat oversimplified because it does not take into account the integumental skeleton, i.e. the scales. In teleostean scales, the superficial osseous layer and the deep basal plate (SIRE, 1987) are both partly (SIRE, 1990), if not completely (SCHUL- TZE, 1977; MEUNIER, 1983, 1984), derived from typical bone tissues. A detailed study of the histological structure of the entire skeleton in the various osteichthyan lineages (endoskeleton on the one hand, exo- skeleton including scales and fin rays on the other hand) indicates that the process of acellularization is a more general feature in scales than in bone sensu stricto. In this way, some relatively primitive lineages, such as the Ostariophysi, show a more or less advanced stage of acellulariza- tion in the scales, whereas the bone has osteocytes (MEUNIER, 1983, 1987).</p>
<p>450 Fig. 8. Recapitulative scheme to show the two main evolutionary trends of bony tissues in Osteichthyes: acellularization (B, E to G) and more or less important lack (see ZYLBERBERG et al., 1991 ) of mineralization (C to G). A: Compact, cellular, vascularized and pseudo-lamellar bone with localized remodelling: Latimeria chalumnae (Crossop- terygii) with three types of osteocytes: a' Acipenser, a" Anguilla, a... Thunnus with a reduced number of cytoplasmic processes; B: Compact, acellular, vascularized with remodelling: Lethrinus nebulosus (Teleostei, Acanthopterygii, Perciformes); C: Cellular osseous and cellular unmineralized permanent 'preosseous' tissues: camptotrichia of Neoceratodusforsteri (Dipnoi, Neoceratodidae); D: Cellular bone and partly unmineralized cellular isopedine: scale of Amia calva; E: Acellular bone and unmineralized cellular isopedine: scale of Latimeria chalumnae and Neoceratodus for.steri; F: Acellular bone and partly unmineralized acellular isopedine: scale of Hemichromis bimaculatus (Teleostei, Acanthopterygii, Perciformes); G: Acellular bone and unmineralized acellular 'pre- osseous' tissue: camptotrichia of Protopterus annectens (Dipnoi, Lepidosirenidae). CM: Mandl's corpuscles; CO: osseous layer; CV I: primary vascular canal; CV II: secondary vascular canal; El: elasmocyte; LAC: rested growth line; LR: reversal cementing line; 0 I: primary bone; 0 II: secondary bone; Osb: osteoblast; Osc: osteoclast; Ost: osteocyte; PB: basal plate. A to G modified from MEUNIER (1987); a' to a'" modified from STEPHAN (1900).</p>
<p>451 As a conclusion we can state that acellularization is a common process in the Osteichthyes (undoubtedly the main group of verte- brates in terms of number of species) (fig. 8). Acellularization is a general trend within the various osteichthyan lineages and especially in Teleostei, where it appears to be a heterochronic phenomenon (MEUNIER, 1987). Within the Teleostei, acellularization is a more general feature in scales than in normal bone: e.g. Salmonidae and Cyprinidae have cellular bone and acellular scales (MEUNIER, 1987); within the Ostariophysi, Characiformes are known with cells (elas- mocytes) included in the basal plate of their scales (Erythrynidae, Anostomidae) whereas Characidae have acellular scales (MEUNIER, 1987). Moreover, in the Teleostei, the more evolved the taxa are (with the exception of the Thunnidae), the more developed is the acellulariz- ation process. The problem of the primacy of cellular or acellular (e.g. aspidin) bone at the beginning of vertebrate history has been dealt with else- where (see, among others, ORVIG, 1967; HALSTEAD, 1969; MEUNIER, 1983; PARENTI, 1986; SMITH & HALL, 1990; SMITH, 1991) and will not be discussed here. However, it should be obvious, as already claimed by 0RIG (1951, 1967), that acellular bone in the Osteichthyes is an apomorphic condition, since it has developed especially in the higher Teleostei; the plesiomorphic condition is cellular bone, which has been maintained in Tretrapoda. THE LOSS OF MINERALIZATION In general, the degree of mineralization of the bony tissues in Osteichthyes is similar to that of mammalian bone (table I). Yet the extreme values obtained for Osteichthyes (0.70 to 1.60 g/cm3) lie wider apart than for mammalian bone (1.15 to 1.50 g/cm3) (see BAUD & POUEZAT, 1973; CASTANET, 1979; MEUNIER, 1983). The degree of mineralization of bone in the Teleostei may be linked to its histological type (cellular or acellular) and to the nature of the aquatic environment (freshwater or marine) (table I), but confirmation is needed (MEUNIER, 1983). Some peculiar skeletal tissues that are homologous with true bone have lost the possibility of mineralization, e.g. the posterior area of the camptotrichia in Dipnoi (GERAUDIE & MEUNIER, 1984) or the basal plate of the elasmoid scales (MEUNIER, 1984) (fig. 8). In the latter case, the structure of the tissues shows typical features of what has been described as isopedine (MEUNIER, 1984; ZYLBERBERG et al., 1991). Some of the most important characteristics of isopedine, besides the extraordinary spatial organization of the collagenous network, are the</p>
<p>452 TABLE I Comparison of the degree of mineralization (in g/cm3) of cellular (+) and acellular (-) bone in various fishes living in fresh (F) or sea (S) water with cellular bone of two amphibians and of man. more or less extensive unmineralized areas and the particular way in which the mineralization front in the basal plate progresses (SIRE, 1987), usually with the presence of Mandl's corpuscles (fig.4). The latter structures, first described by BAUDELOT (1873 a,b), are calcified concretions showing a great variability of form (e.g. ovoid, cubic, polyhedral and spherical) according to the species considered (SCHON- BORNER et al., 1981 ) and according to the 'plywood' type characteriz- ing the basal plate (MEUNIER, 1984). Furthermore, in certain cases these unmineralized tissues have also lost their osteocytes: in the camptotrichia as well as in the isopedine (GERAUDIE & MEUNIER, 1984; MEUNIER, 1983, 1987). We therefore end up with cases of skeletal tissues having a similar origin and/or function to bone but lacking both mineral and osteocytes (fig. 8). In view of these findings, it is difficult to adhere to the currently adopted concept of bone tissue as a collection of specialized cells, some of which produce (and then become embedded in) a network of collagenous fibres supporting a solid phase of minerals. Two further examples illustrate the very close relationship between bone and unmineralized (possibly acellular) isopedine. In the scales of the coelacanth, the mineral component of the isopedine is missing, but in the lateral line scales, the basal plate has vascular canals as in bone (MEUNIER, 1980) and remodelling areas where typical bone lies close</p>
<p>453 to unmineralized isopedine (fig. 5). In the same species, the anterioir bony part of the post-temporal merges relatively imperceptibly (with- out clear limits such as cement lines) with the posterior isopedine part. Moreover, it seems to be the same scleroblast population which gives the cellular mineralized bone and the cellular unmineralized isopedine (MEUNIER, 1980). TELEOST CHONDROID BONE Another type of skeletal tissue which balances at the limit of the classical definitions, and which is frequently found in articular areas in the head of teleosts, is chondroid bone. Mature chondroid bone is a skeletal tissue with large, haphazardly dispersed chondrocyte-like cells embedded in a mineralized bone-like matrix (figs 6-7, 9). Chondroid bone, such as that supporting the articular facets of the upper pharyngeal jaws in Cichlidae, forms when osteoblasts, instead of retracting (as osteoblasts normally do when forming acellular bone), become trapped in the bone-like matrix they deposit (HUYSSEUNE, 1986). Young chondroid bone thus resembles young cellular bone (without osteocytic prolongations), but changes in the matrix composi- tion (especially an increase in acid carbohydrates) and acquisition of a chondrocytic instead of an osteocytic phenotype of the trapped cells, soon give the tissue an appearance intermediate between cartilage and bone (HuYSSEUNE & VERRAES, 1986, 1990). Chondroid bone thus forms de mono from osteogenic precursors, not by transformation of an existing tissue, implying that there is no metaplasia involved. Both young and mature chondroid bone are overlaid superficially with a so-called fibrous articular layer, consisting of fibroblasts and cells providing the progenitors for the chondroid bone. A narrow unmineralized layer forms the transition towards the chondroid bone proper (figs 6-7, 9). In its deep part, chondroid bone is broken down by multinucleated osteoclasts, but new bone may be deposited against the resorption front. At its sides, chondroid bone remains unaffected by erosion and merges without cement lines with the bone of the element on which it has developed (figs 6, 9). Turnover of the chondroid bone results in a shift in its position, and in this way chondroid bone contributes to the growth of the bony element proper, as illustrated by HUYSSEUNE & VERRAES (1986), HUYSSEUNE el al. (1986) and in fig. 9. The lack of cement lines between chondroid bone and (acellular or cellular) bone furthermore confirms their related structure, and sug- gests that one population of progenitor cells may be responsible for the formation of both tissues.</p>
<p>454 Fig. 9. Schematic drawing of the structure and localization of chondroid bone on an acellular bony element. Open and solid arrow respectively indicate the direction of resorption and deposition. Dotted lines and small arrows indicate the shift in position when chondroid bone grows distally while being broken down proximally. ABBREVIATIONS AB: acellular bone; ac: articular cavity; CB: chondroid bone; cc: chondroid bone cell; m: medullary cavity; mm: mineralized matrix of the chondroid bone; oc: osteoclast; op: osteoprogenitor cell; um: unmineralized matrix of chondroid bone. Chondroid bone can be anything between almost acellular (e.g. on the maxillary of rainbow trout) and highly cellular (e.g. on cichlid pharyngeal jaws), and therefore the resemblance to cartilage can be less or more pronounced. In its highly cellular from, chondroid bone resembles (mineralized) secondary cartilage, but is distinguished from it by its fine structure (HUYSSEUNE & SIRE, 1990), its histochemical properties (HUYSSEUNE & VERRAES, 1990), as well as by immu- nofluorescence and microradiographical data (HUYSSEUNE, 1989). A survey of the head of juvenile and adult specimens of the cichlid Astatotilapia elegans reveals that chondroid bone is usually, but not necessarily, present in joints. Although chondroid bone matrix resembles matrix of woven bone, the incorporation of a large number of cells will almost certainly have a weakening effect. It is possible that chondroid bone, like mammalian woven bone with its fairly spherical osteocyte lacunae, is adapted "for speed of reconstruction, not mechanical excellence" (CURREY, 1984). It would indeed appear that chondroid bone combines the need for an accelerated local growth rate with the demand for a shear-resistant</p>
<p>455 skeletal support. Clearly, the examination of distant species varying in the amount of chondroid bone on homologous elements will prove very helpful. Similarly, the study of teleost families (e.g. Cichlidae) that assemble species of considerably different feeding types (and therefore possessing different kinematic patterns and force regimes) can provide a firm basis to explain the functional significance of chondroid bone. From a preliminary survey of Teleostei, it would appear that chondroid bone is more frequent in advanced teleosts, i.e. in teleosts that generally have an acellular bone skeleton (although one must bear in mind that finding chondroid bone in cellular-boned fishes such as eel, carp and trout, is frequently hampered by the lack of a clear-cut limit between ordinary cellular bone and cell-poor chondroid bone). One hypothesis is that chondroid bone evolved from cellular bone, by an increased rate of incorporation of cells, along with a change in their metabolic properties. The development of such a tissue would have allowed the rapid outgrowth of an articular process or apophysis (cf. HUYSSEUNE et al., 1986). The presence of matrix vesicles ahead of the mineralization front, which is generally admitted to be associated with areas of fast mineralization, is in agreement with this hypothesis. Summarizing, chondroid bone in Teleostei is found in joints and in sites subjected to mechanical stress and seems to meet two demands (sensu DULLEMEIJER, 1974): (1) demands of movement, requiring the adjustment of the shape of the bone (formation of an articular process, apophysis), which probably can be rapidly achieved by the incorpora- tion of cells, and (2) demands of support and resistance (presumably to shear stresses); the latter may explain the particular matrix properties and the chondrocytic phenotype of the cells. We disagree with VINKKA (1982) that chondroid bone forms as the outcome of incomplete differentiation by lack of appropiate stimuli. Rather, our developmental, morphological and histochemical data indicate that chondroid bone is a fully differentiated and functional tissue. CONCLUSION The evolutionary trends of acellularization and loss of capacity of mineralization are linked to the general regression of the dermal skeleton in most osteichthyan lineages since the Palaeozoic Era on the one hand, and to a functional adaption on the other hand. This is especially the case for isopedine which, to a greater or lesser extent, has undergone specializations (at least with respect to the mineral content) in relation to an improved hydrodynamic efficiency of the fish. These evolutionary changes within the Osteichthyes have led to the</p>
<p>456 emergence of a continuum of skeletal tissues, form bone and bone- derived tissues at one extreme to cartilages at the other, blurring the classical clear-cut limits between generally adopted categories of con- nective tissues. Isopedine and chondroid bone provide only a few examples of such tissues, more examples being given by, among others, SCHAFFER (1930), ORVIG (1951, 1967) and BENJAMIN (1990). Each tissue type represents the result of developmental and functional (mechanical, spatial) constraints, which are probably more diverse in Osteichthyes than in Tetrapoda. Their formation is mediated by spe- cific metabolic and biochemical factors acting on the scleroblasts which produce these tissues. So far, evidence for epigenetic influences on skeletal differentiation in teleosts is still virtually non-existent, but is presaged by experimental evidence for such influences in tetrapods (e.g. the mechanical evocation of secondary cartilages, see HALL, 1984). We can only regret the great scarcity of physiological studies in relation to these bone and bone-derived tissues. Such knowledge would undoubtedly contribute to a better understanding of their physiologi- cal function and of the evolutionary history of their development. It would probably also make it easier to comprehend the respective roles of genetics and of epigenetical constraints in the achievement of the particularly rich variety of bone-derived tissues in bony fishes. REFERENCES BAUD, C.A. & J.A. POUEZAT, 1973. Données microradiographiques quantitatives sur le minéral osseux dans l'ostéoporose post-traumatique. Rhumatologie 25: 75-77. BAUDELOT, M.E., 1873a. Recherches sur la structure et le développement des écailles des poissons osseux. Première partie. Arch. Zool. Exp. Gén. 2: 87-244. BAUDELOT, M.E., 1873b. Recherches sur la structure et le développement des écailles des poissons osseux. Deuxième partie. Arch. Zool. Exp. Gén. 2: 429-480. BENJAMIN, M., 1990. The cranial cartilages of teleosts and their classification. J. Anat. 169: 153-172. BERESFORD, W.A., 1981. Chondroid bone, secondary cartilage and metaplasia. Urban and Schwarzenberg, Baltimore. BLANC, M., 1953. Contribution à l'étude de l'ostéogenèse chez les Poissons Téléostéens. Mém. Mus. Nat. Hist. Nat. 7: 1-145. CASTANET, J., 1979. Données comparatives sur la minéralisation des marques de croissance squelettique chez les Vertébrés. Etude par microradiographie quantita- tive. C.R. Acad. Sci. 289: 405-408. CURREY, J., 1984. The mechanical adaptations of bones. Princeton University Press, Prince- ton, New Yersey. DULLEMEIJER, P., 1974. Concepts and approaches in animal morphology. Van Gorcum & Co., Assen, The Netherlands. FRANCILLON-VIEILLOT, H., V. DE BUFFRENIL, J. CASTANET, J. GERAUDIE, F.J. MEUNIER, J.-Y. SIRE, L. ZYLBERBERG & A. DE RICQLES, 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: J.G. CARTER (Ed.): Skeletal biomineralization: Patterns, processes and evolutionary trends, Vol. I: 471-530. Van Nos- trand Reinhold, New York.</p>
<p>457 GERAUDIE, J. & F.J. MEUNIER, 1984. Structure and comparative morphology of cam- ptotrichia of lungfish fins. Tissue and Cell 16: 217-236. HALL, B.K., 1984. Genetic and epigenetic control of connective tissues in the craniofa- cial structures. Birth Defects, Orig. Article Ser. 20: 1-17. HALSTEAD, L.B., 1969. Calcified tissues in the earliest vertebrates. Calcif. Tissue Res. 3: 107-124. HUYSSEUNE, A., 1986. Late skeletal development at the articulation between upper pharyngeal jaws and neurocranial base in the fish, Astatotilapia elegans, with the participation of a chondroid form of bone. Am. J. Anat. 177: 119-137. HUYSSEUNE, A., 1989. Morphogenetic aspects of the pharyngeal jaws and neurocranial apophysis in postembryonic Astatotilapia elegans (Trewavas, 1933) (Teleostei : Cich- lidae). Academiae Analecta (Brussels) 51: 11-35. HUYSSEUNE, A. & J.-Y. SIRE, 1990. Ultrastructural observations on chondroid bone in the teleost fish Hemichromis bimaculatus. Tissue & Cell 22: 371-383. HUYSSEUNE A. & W. VERRAES, 1986. Chondroid bone on the upper pharyngeal jaws and neurocranial base in the adult fish Astatotilapia elegans. Am. J. Anat. 177: 527-535. HUYSSEUNE A. & W. VERRAES, 1990. Carbohydrate histochemistry of mature chondroid bone in Astatotilapia elegans (Teleostei : Cichlidae) with a comparison to acellular bone and cartilage. Ann. Sci. Nat., Zool., 13e Série 11: 29-43. HUYSSEUNE, A., W. VANDEN BERGHE & W. VERRAES, 1986. The contribution of chondroid bone in the growth of the parasphenoid bone of a cichlid fish as studied by oblique computer-aided reconstructions. Biol. Jb. Dodonaea 54: 131-141. KOLLIKER, A., 1859. On the different types in the microscopic structure of the skeleton of osseous fish. Proc. R. Soc. Lond. 9: 656-688. MEUNIER, F.J., 1980. Les relations isopédine-tissu osseux dans le post-temporal et les écailles de la ligne latérale de Latimeria chalumnae (Smith). Zool. Scripta 9: 307-317. MEUNIER F.J., 1983. Les tissus osseux des Ostéichthyens. Structure, genèse, croissance et évolution. Arch. Doc. Inst. Ethnol., micro-édition, Mus Nat. Hist. Nat., SN 82-600-328, 200 pp. MEUNIER, F.J., 1984. Spatial organization and mineralization of the basal plate of elasmoid scales in Osteichthyans. Amer. Zool. 24: 953-964. MEUNIER, F.J., 1987. Os cellulaire, os acellulaire et tissus dérivés chez les Ostéichthyens: les phénomènes de l'acellularisation et de la perte de minéralisa- tion. Ann. Biol. 26: 201-233. Moss, M.L., 1961 a. Studies of the acellular bone of teleost fish. I- Morphological and systematic variations. Acta Anat. 46: 343-362. Moss, M.L., 1961b. Osteogenesis of acellular teleost fish bone. Amer. J. Anat. 108: 99-110. Moss, M.L., 1963. The biology of acellular teleost bone. Ann. N.Y. Acad. Sci. 109: 337-350. Moss, M.L., 1965. Studies of the acellular bone of teleost fish. V- Histology and mineral homeostasis of fresh-water species. Acta Anat. 60: 262-276. ØRVIG, T., 1951. Histologic studies of Placoderms and fossil Elasmobranchs. I. The endoskeleton, with remarks on the hard tissue of lower vertebrates in general. Ark. Zool. 2: 321-454. ØRVIG, T., 1967. Phylogeny of tooth tissues : evolution of some calcified tissues in early vertebrates. In: A.E.W. MILES (Ed.): Structural and chemical organization of teeth, Vol. I: 45-105. Academic Press, New York. PARENTI, L.R., 1986. The phylogenetic significance of bone types in euteleost fishes. Zool. J. Linn. Soc. 87: 37-51. PETERSEN, H., 1930. Die Organe des Skelettsystems. In: W. VON MOLLENDORFF (Ed.):</p>
<p>458 Handbuch der mikroskopischen Anatomie des Menschen: 521-678. Julius Springer, Berlin. RICQLES, A. DE, 1975. Recherches paléohistologiques sur les os longs des Tétra- podes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des Tétrapodes (1ère Part.). Ann. Paléont. 61: 51-81. RICQLES, A. DE, F.J. MEUNIER, J. CASTANET & H. FRANCILLON-VIEILLOT, 1991. Comparative Microstructure of Bone. In: B.K. HALL (Ed.): Bone : a Treatise, Vol. 3: 1-78. CRC Press, Boca Raton, Florida. SCHAFFER, J., 1930. Die Stützgewebe. In: W. VON MÖLLENDORFF (Ed.): Handbuch der Mikroskopischen Anatomie des Menschen, II(2): 1-390. Julius Springer, Berlin. SCHÖNBÖRNER, A.A., F.J. MEUNIER & J. CASTANET, 1981. The fine structure of calcified Mandl's corpuscles in teleost fish scales. Tissue and Cell 13: 589-597. SCHULTZE, H.P., 1977. Ausgangsform und Entwicklung der rhombischen Schuppen der Osteichthyes (Pisces). Paläont. Z. 51 : 152-168. SIRE, J.-Y., 1987. Structure, formation et régénération des écailles d'un poisson téléostéen, Hemi- chromis bimaculatus (Perciforme, Cichlide). Arch. Doc. Inst. Ethnol., micro-édition, Mus. Nat. Hist. Nat., SN 87-600-449, 262 pp. SIRE, J.-Y., 1990. From ganoid to elasmoid scales in the Actinopterygian fishes. Neth. J. Zool. 40: 75-92. SMITH, M.M., 1991. Putative theletal neural crest cells in early late-Ordovician Verte- brates from Colorado. Science 251: 301-303. SMITH, M.M. & B.K. HALL, 1990. Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65: 277-373. STEPHAN, P., 1900. Recherches histologiques sur la structure du tissu osseux des Poissons. Bull. Scient. Fr. Belg. 33: 281-429. VINKKA, H., 1982. Secondary cartilages in the facial skeleton of the rat. Proc. Finn. Dent. Soc. 78, Suppl. VII: 1-137. WEISS, R.E. & N. WATABE, 1979. Studies on the biology of fish bone. III- Ultrastruc- ture of osteogenesis and resorption in osteocytic (cellular) and anosteocytic (acellu- lar) bones. Calc. Tiss. Intern. 28: 43-56. WILLIAMSON, W.C., 1851. Investigations into the structure and development of the scales and bones of fishes. Phil. Trans. Roy. Soc. Lond. 141: 643-702. ZYLBERBERG, L., J. GERAUDIE, F. J. MEUNIER &J.-Y. SIRE, 1991. Biomineralization in the integumental skeleton of the living lower vertebrates. In: B.K. HALL (Ed.): Bone : a Treatise, Vol. 4: 171-224. CRC Press, Boca Raton, Florida.</p>
</body></article></istex:document></istex:metadataXml><mods version="3.6"><titleInfo><title>The Concept of Bone Tissue in Osteichthyes</title></titleInfo><titleInfo type="alternative" contentType="CDATA"><title>The Concept of Bone Tissue in Osteichthyes</title></titleInfo><name type="personal"><namePart type="given">Francois J.</namePart><namePart type="family">Meunier</namePart><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">Ann</namePart><namePart type="family">Huysseune</namePart><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="research-article" displayLabel="research-article"></genre><originInfo><publisher>BRILL</publisher><place><placeTerm type="text">The Netherlands</placeTerm></place><dateIssued encoding="w3cdtf">1991</dateIssued><dateCreated encoding="w3cdtf">1991</dateCreated><copyrightDate encoding="w3cdtf">1991</copyrightDate></originInfo><language><languageTerm type="code" authority="iso639-2b">eng</languageTerm><languageTerm type="code" authority="rfc3066">en</languageTerm></language><physicalDescription><internetMediaType>text/html</internetMediaType></physicalDescription><subject><genre>keywords</genre><topic>mineralization</topic><topic>bone</topic><topic>Osteichthyes</topic><topic>acellularization</topic><topic>chrondroid bone</topic><topic>isopedine</topic></subject><relatedItem type="host"><titleInfo><title>Netherlands Journal of Zoology</title></titleInfo><titleInfo type="abbreviated"><title>NJZ</title></titleInfo><genre type="journal">journal</genre><identifier type="ISSN">0028-2960</identifier><identifier type="eISSN">1568-542X</identifier><part><date>1991</date><detail type="volume"><caption>vol.</caption><number>42</number></detail><detail type="issue"><caption>no.</caption><number>2-3</number></detail><extent unit="pages"><start>445</start><end>458</end></extent></part></relatedItem><identifier type="istex">6CA54C31B1AE225B8033DC8BCAE83B8CF1898482</identifier><identifier type="DOI">10.1163/156854291X00441</identifier><identifier type="href">1568542x_042_02-03_s022_text.pdf</identifier><accessCondition type="use and reproduction" contentType="copyright">© 1991 Koninklijke Brill NV, Leiden, The Netherlands</accessCondition><recordInfo><recordContentSource>BRILL Journals</recordContentSource><recordOrigin>Koninklijke Brill NV, Leiden, The Netherlands</recordOrigin></recordInfo></mods></metadata><serie></serie></istex></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Wicri/Eau/explor/EsturgeonV1/Data/Istex/Corpus
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000359 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Istex/Corpus/biblio.hfd -nk 000359 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Wicri/Eau
|area= EsturgeonV1
|flux= Istex
|étape= Corpus
|type= RBID
|clé= ISTEX:6CA54C31B1AE225B8033DC8BCAE83B8CF1898482
|texte= The Concept of Bone Tissue in Osteichthyes
}}
| This area was generated with Dilib version V0.6.27. |  |