THE CONCEPT OF BONE TISSUE IN OSTEICHTHYES

by

FRANCOIS J. MEUNIER1 and ANN HUYSSEUNE2 (1 Laboratoired'Ichtyologie, Muséum National d'HistoireNaturelle, 43 rue Cuvier,75231 Paris Cédex 05, France, and Equipe de Recherche'Formations Squelettiques, URA CNRS 1134, UniversitéParis 7, 2 placeJussieu, 75251 Paris Cédex05, France. 2 Seniorresearch assistant, Institut voorDierkunde, 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,LESet al. ( 1991 and) ZYLBERBERG al.et ( 1991 ). 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,