Bull. Kitakyushu Mus. Nat. Hist. Hum. Hist., Ser. A, 17: 37–48, March 31, 2019

The skeleton and the mineralized tissues of the living coelacanths elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. Origin of extant composed of the notochord which is coated by an unmineralized basal plate, where spheritic mineralized granules are seen in al., 2015, 2019). AGASSIZ, L. 1833–44. Recherches sur les Poissons fossiles. Morphology, 275: 841–861. DOI: 10.1002/jmor.20258 855–858. interrelationships. Cybium, 42: 41–65. 28: 1–106, 44 Pls. coelacanths. The Coelacanth, Fathom the Mystery 2007. EUNIER1 UPELLO2 LÉMENT3 François J. M , Camila C and Gaël C fibrillary sheath and is totally deprived of well developed the very first layers of the basal plate (MEUNIER, 1980; Imprimerie Petitpierre, Neuchâtel. [5 volumes and atlas.] ERDMANN, M. V., CALDWELL, R. L. and MOOSA, M. K. 1998. HUREAU J.-Cl. and OZOUF, C. 1977. Détermination de l’âge et ØRVIG T. 1951. Histologic studies of Placoderms and fossil SMITH, M. M. 1978. Enamel in the oral teeth of Latimeria Aquamarine Fukushima, pp. 24–26. vertebrae due to the lack of ossified centra, although some MEUNIER and ZYLBERBERG, 1999; MEUNIER et al., 2008). There ANDREWS, S. M. 1973. Interrelationships of crossopterygians. Indonesian “king of the sea” discovered. Nature, 395: croissance du cœlacanthe Latimeria chalumnae SMITH, Elasmobranchs. 1: The endoskeleton, with remarks on the chalumnae (Pisces: Actinistia): a scanning electron ZYLBERBERG, L. and MEUNIER, F. J. 2008. New data on the 1 UMR 7208 (MNHN - Sorbonne Universités - Univ. Caen Normandie - Univ. Antilles – CNRS - IRD), discrete neural and haemal arches develop in the anterior part is no pore-canal system so Latimeria’s scales are not cosmoid, CONCLUSION In: GREENWOOD, P. H., MILES, R. S. and PATTERSON, C. 335. 1939 (Poisson, Crossoptérygien, Coelacanthidé). Cybium, hard tissues of lower vertebrates in general. Arkiv för microscopic study. Journal of Zoology, 185: 355–369. structure and the chondrocyte populations of the haemal BOREA, Département Adaptations du Vivant, Muséum national d'Histoire naturelle, C.P. 026, 43 rue Cuvier, of the notochord (MILLOT and ANTHONY, 1958). The anterior contrary to most of palaeozoic sarcopterygian fishes. Due to (eds.), Interrelationships of Fishes, Acad. Press, London, ERDMANN, M. V., CALDWELL, R. L., JEWETT, S. L. and 2: 129–137. Zoologi, 2: 321–454, 8 pl. SMITH, M. M. 1979. Scanning electron microscopy of cartilage of abdominal vertebrae in the adult carp 75231 Paris cedex 05, France. E-mail: [email protected] neural and haemal spines are relatively short but they the presence of an unmineralized stratified basal plate, the This overview of eighty years (1938–2018) of histological pp. 137–177. TJAKRAWIDJAJA, A. 1999. The second recorded living JANVIER, P. 1996. Early Vertebrates. Clarendon Press, Oxford, ØRVIG T. 1968. The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). 2Departamento de Zoologia, Universidade do Estado do Rio de Janeiro, R. São Francisco Xavier, 524-Maracanã, Rio de Janeiro 20550–900, Brazil. E-mail: [email protected] progressively increase in length posteriorly. Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. 3UMR 7207 (MNHN–Sorbonne Université–CNRS), Centre de Recherche sur la Paléobiodiversité et les and haemal spines are composed of perichondral bone However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., Paléoenvironnements, Département Origines & Evolution, Muséum national d’Histoire naturelle, CP38, 57 surrounding a cartilaginous core (Fig. 2). homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of rue Cuvier, 75231 Paris cedex 05, France. E-mail: [email protected] The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, (Received August 12, 2018; accepted October 22, 2018) and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria ABSTRACT − The present overview of the histological studies on Latimeria mineralized tissues, since the external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia discovery of the first living coelacanth in 1938, allows some anatomical and evolutionary considerations. It area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). enlightens: i) a drastic reduction of cartilage to bone transformation processes during evolution; ii) the persistence denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., of large volume of cartilage in the endoskeleton at adult stage; iii) the bony nature of the plates that surround the 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. lung diverticle; iv) the presence of a developed process of spheritic mineralization in various skeletal organs: in the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques teeth, in odontodes of the tegumentary skeleton (scales, fin rays), in scales at the interface between the external been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des layer and the basal plate, as well as in lung bony plates. ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 38 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 39

elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. 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SMITH, M. M. 1979. Scanning electron microscopy of cartilage of abdominal vertebrae in the adult carp neural and haemal spines are relatively short but they the presence of an unmineralized stratified basal plate, the This overview of eighty years (1938–2018) of histological pp. 137–177. TJAKRAWIDJAJA, A. 1999. The second recorded living JANVIER, P. 1996. Early Vertebrates. Clarendon Press, Oxford, ØRVIG T. 1968. The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). progressively increase in length posteriorly. Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. and haemal spines are composed of perichondral bone However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., surrounding a cartilaginous core (Fig. 2). homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have Fig. 3. Latimeria chalumnae and L. menadoensis. Details of the posterior field of scales (SEM). A, L. chalumnae. General view of MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for the odontodes. The posterior margin of the scale is on the upper left. (scale = 500 µm). B, L. menadoensis. General view of the girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). odontodes. The posterior margin of the scale is on the upper right. (scale = 500 µm). C, L. menadoensis. Closed-up view of the is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of odontodes positioned on the radial crests of the external layer. (scale = 100 µm). D, L. chalumnae. Closed-up view of the bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: odontodes positioned on the radial crests of the external layer, and two superimposed odontodes are seen on the right (*). is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in (scale = 100 µm). E, L. chalumnae. Closed-up view of two superimposed odontodes with the apical part of the lower one being ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). eroded (arrow). (scale = 100 µm). (After MEUNIER et al., 2008). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, Fig. 1. Schematic phylogeny of nine fossil genera of Actinistia 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, and the extant Latimeria. (modified from CASANE and A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON LAURENTI, 2013, fig. 1). abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins Fig. 2. Latimeria chalumnae. Skeleton (bones, cartilages and fin rays) of entire fish based on MILLOT and ANTHONY (1958) and Fig. 4. Latimeria chalumnae. Buccal roof showing the different tooth types: fangs (black arrow-heads), small caniniform teeth (white and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements after FOREY (1998). Note i) the monobasal insertion of pectoral, pelvic, anal and second dorsal fins on their respective girdle; arrow-heads) and patches of round shaped teeth (black arrows), especially on the parasphenoid tooth plate (t.par) and the medial (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial ii) the presence of minute neural and haemal arches (respectively arrow-heads and arrows). (Scale = 100 mm). side of the pterygoid (t.pt). The front side is on the top of the figure. (After MILLOT and ANTHONY, 1958). (scale = 10 mm). MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 38 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 39 elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. Origin of extant composed of the notochord which is coated by an unmineralized basal plate, where spheritic mineralized granules are seen in al., 2015, 2019). AGASSIZ, L. 1833–44. 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Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have Fig. 3. Latimeria chalumnae and L. menadoensis. Details of the posterior field of scales (SEM). A, L. chalumnae. General view of MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for the odontodes. The posterior margin of the scale is on the upper left. (scale = 500 µm). B, L. menadoensis. General view of the girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). odontodes. The posterior margin of the scale is on the upper right. (scale = 500 µm). C, L. menadoensis. Closed-up view of the is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of odontodes positioned on the radial crests of the external layer. (scale = 100 µm). D, L. chalumnae. Closed-up view of the bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: odontodes positioned on the radial crests of the external layer, and two superimposed odontodes are seen on the right (*). is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in (scale = 100 µm). E, L. chalumnae. Closed-up view of two superimposed odontodes with the apical part of the lower one being ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). eroded (arrow). (scale = 100 µm). (After MEUNIER et al., 2008). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, Fig. 1. Schematic phylogeny of nine fossil genera of Actinistia 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, and the extant Latimeria. (modified from CASANE and A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON LAURENTI, 2013, fig. 1). abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins Fig. 2. Latimeria chalumnae. Skeleton (bones, cartilages and fin rays) of entire fish based on MILLOT and ANTHONY (1958) and Fig. 4. Latimeria chalumnae. Buccal roof showing the different tooth types: fangs (black arrow-heads), small caniniform teeth (white and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements after FOREY (1998). Note i) the monobasal insertion of pectoral, pelvic, anal and second dorsal fins on their respective girdle; arrow-heads) and patches of round shaped teeth (black arrows), especially on the parasphenoid tooth plate (t.par) and the medial (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial ii) the presence of minute neural and haemal arches (respectively arrow-heads and arrows). (Scale = 100 mm). side of the pterygoid (t.pt). The front side is on the top of the figure. (After MILLOT and ANTHONY, 1958). (scale = 10 mm). MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 40 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 41 elements and eventually minute superficial endochondral Fig. 6. Latimeria chalumnae. Bone histology. A, Thin section 2008). 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K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have D, Ground section of the angular, in a deeper region than MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for C. Several bulks of secondary bone (sb) are limited by girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). cementing lines (black arrow-heads). Primary bone (pb) is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of persists in different areas. The white asterisks point to bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: secondary vascular cavities. (scale = 200 µm). (C, D: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in After FRANCILLON et al., 1975). ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., Fig. 5. Latimeria chalumnae. Coronoid and coronoid tooth structure. A, Tomographic imaging of a coronoid element. 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., Three-dimensional reconstruction of the dental plate showing a fang, one mid-sized caniniform tooth (*) and numerous small The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). round-shaped teeth (arrow-heads). The virtual section shows i) the plies of the dentine in the lower half of the pulp cavity (pc); fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ii) the bone of attachment (ba) between the tooth and the coronoid bony tissue. On the right of the figure, the coronoid shows a ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones network of vascular cavities and canals (vc). (de = dentine; en = enamel) (scale = 1 mm). (After MEUNIER et al., 2015, Fig. These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were 9-10). B, Microradiography of a cross section at the base of a fang showing several plies of the dentine wall (white Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth arrow-heads). (bo = bone; pc = pulp cavity; de = dentine). (scale = 1 mm). (from CASTANET et al., 1975). C, Scanning Electron Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria Microscopy of the spheritic dentine. The white and black asterisks point respectively to the external surface of the tooth and to primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and the wall of the pulp cavity. (scale = 25 µm). heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 40 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 41 elements and eventually minute superficial endochondral Fig. 6. Latimeria chalumnae. Bone histology. A, Thin section 2008). 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The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). progressively increase in length posteriorly. Importantly neural membrane (white arrows). On the right, numerous scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. and haemal spines are composed of perichondral bone collagenous fibres (cf) enter the bony matrix where they However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., surrounding a cartilaginous core (Fig. 2). form SHARPEY’s fibres. The asterisks points to secondary homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of The scales belong to the exoskeleton. In both extant vascular cavities limited by cementing lines (white extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an arrow-heads); a primary vascular canal (vc) is seen. (scale HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, = 100 µm). C, X-ray ground section in the cortical region Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is of the angular showing primary bone with regular The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper alternative of heterogeneous mineralized bony tissue. The by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior black arrow-heads point to primary vascular canals, the fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous white arrows to cementing lines, and the white ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. arrow-heads to erosive bays. The asterisks point to two an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by confluent secondary vascular cavities). (scale = 200 µm). been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have D, Ground section of the angular, in a deeper region than MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for C. Several bulks of secondary bone (sb) are limited by girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). cementing lines (black arrow-heads). Primary bone (pb) is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of persists in different areas. The white asterisks point to bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: secondary vascular cavities. (scale = 200 µm). (C, D: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in After FRANCILLON et al., 1975). ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., Fig. 5. Latimeria chalumnae. Coronoid and coronoid tooth structure. A, Tomographic imaging of a coronoid element. 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., Three-dimensional reconstruction of the dental plate showing a fang, one mid-sized caniniform tooth (*) and numerous small The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). round-shaped teeth (arrow-heads). The virtual section shows i) the plies of the dentine in the lower half of the pulp cavity (pc); fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ii) the bone of attachment (ba) between the tooth and the coronoid bony tissue. On the right of the figure, the coronoid shows a ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones network of vascular cavities and canals (vc). (de = dentine; en = enamel) (scale = 1 mm). (After MEUNIER et al., 2015, Fig. These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were 9-10). B, Microradiography of a cross section at the base of a fang showing several plies of the dentine wall (white Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth arrow-heads). (bo = bone; pc = pulp cavity; de = dentine). (scale = 1 mm). (from CASTANET et al., 1975). C, Scanning Electron Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria Microscopy of the spheritic dentine. The white and black asterisks point respectively to the external surface of the tooth and to primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and the wall of the pulp cavity. (scale = 25 µm). heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 42 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 43 elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. Origin of extant composed of the notochord which is coated by an unmineralized basal plate, where spheritic mineralized granules are seen in al., 2015, 2019). AGASSIZ, L. 1833–44. 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Scanning electron microscopy of cartilage of abdominal vertebrae in the adult carp neural and haemal spines are relatively short but they the presence of an unmineralized stratified basal plate, the This overview of eighty years (1938–2018) of histological pp. 137–177. TJAKRAWIDJAJA, A. 1999. The second recorded living JANVIER, P. 1996. Early Vertebrates. Clarendon Press, Oxford, ØRVIG T. 1968. The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). progressively increase in length posteriorly. Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. and haemal spines are composed of perichondral bone However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., surrounding a cartilaginous core (Fig. 2). homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for Fig. 7. Latimeria menadoensis and L. chalumnae. Ground sections of scales. A, L. menadoensis. Longitudinal section; X-ray. The girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). superficial bony layer (bo) and the odontodes (arrow-heads) are mineralized whereas the basal plate (BP) totally lacks is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of mineralization (asterisks). Vascular canals are present within the superficial bony layer. The arrow on the upper right indicates bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: the direction of the head. B–C, L. chalumnae. Transversal sections; respectively polarized light and X-ray. B, The basal plate is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in is made of stratified layers of collagenous fibres (arrow). The arrow-heads point to the superficial odontodes. C, The ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). superficial bony layer and the odontodes (arrow-heads) are mineralized whereas the basal plate (BP) totally lacks the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp mineralization (asterisks). D, L. chalumnae. Longitudinal section; X-ray. The superficial bony layer (bo) and the odontodes ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). (arrow-head) are mineralized whereas the basal plate (BP) totally lacks mineralization (asterisks). (af = anterior field; pf = constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., posterior field). E, L. menadoensis. Broken frozen scale showing the different fibres directions in the successive layers of the ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). basal plate. The rotation of the fibres directions from one layer to another characterizes a plywood-like organization. The Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., arrow points to the crests of the superficial layer. (A, B, C: scale = 1 mm; D: scale = 2 mm; E: scale = 200 µm). (B, C, D after The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). CASTANET et al., 1975; A, E after MEUNIER et al., 2008). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, Fig. 8. Latimeria chalumnae. Cartilage histology (after SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of FRANCILLON et al., 1975). A, MECKEL’s cartilage (thin revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). histological section; Hemalun-PIC staining). An erosive periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells vascular cavity (black asterisk) is separated from the 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the medullary cavity (mc) by a layer of enchondral bone (eb). SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the Elongate chondrocytes (arrow-heads) are seen in the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific cartilage. (scale = 50 µm). B, Scapulocoracoid (ground as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and section 3 mm thick; x-ray). The cartilage (ca) is invaded by fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. resorption canals (white asterisks), their wall is covered by In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement thin bony layers, here clearly visible in white colour. The series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The white arrow-heads point to the erosion front of the cartilage. at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a (scale = 1 mm). C, Scapulocoracoid (thin histological half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is section; Stoelzner staining). In the cartilage (ca), the present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the vascular cavities (vc), resulting from a chondroclastic (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its activity, are bordered by thin bony lamellae here visible characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., in black colour (arrow-heads). (scale = 250 µm). These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 42 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 43 elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. Origin of extant composed of the notochord which is coated by an unmineralized basal plate, where spheritic mineralized granules are seen in al., 2015, 2019). AGASSIZ, L. 1833–44. 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Scanning electron microscopy of cartilage of abdominal vertebrae in the adult carp neural and haemal spines are relatively short but they the presence of an unmineralized stratified basal plate, the This overview of eighty years (1938–2018) of histological pp. 137–177. TJAKRAWIDJAJA, A. 1999. The second recorded living JANVIER, P. 1996. Early Vertebrates. Clarendon Press, Oxford, ØRVIG T. 1968. The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). progressively increase in length posteriorly. Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. 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Biomineralization in the integumental skeleton of The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for Fig. 7. Latimeria menadoensis and L. chalumnae. Ground sections of scales. A, L. menadoensis. Longitudinal section; X-ray. The girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). superficial bony layer (bo) and the odontodes (arrow-heads) are mineralized whereas the basal plate (BP) totally lacks is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of mineralization (asterisks). Vascular canals are present within the superficial bony layer. The arrow on the upper right indicates bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: the direction of the head. B–C, L. chalumnae. Transversal sections; respectively polarized light and X-ray. B, The basal plate is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in is made of stratified layers of collagenous fibres (arrow). The arrow-heads point to the superficial odontodes. C, The ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). superficial bony layer and the odontodes (arrow-heads) are mineralized whereas the basal plate (BP) totally lacks the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp mineralization (asterisks). D, L. chalumnae. Longitudinal section; X-ray. The superficial bony layer (bo) and the odontodes ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). (arrow-head) are mineralized whereas the basal plate (BP) totally lacks mineralization (asterisks). (af = anterior field; pf = constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., posterior field). E, L. menadoensis. Broken frozen scale showing the different fibres directions in the successive layers of the ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). basal plate. The rotation of the fibres directions from one layer to another characterizes a plywood-like organization. The Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., arrow points to the crests of the superficial layer. (A, B, C: scale = 1 mm; D: scale = 2 mm; E: scale = 200 µm). (B, C, D after The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). CASTANET et al., 1975; A, E after MEUNIER et al., 2008). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, Fig. 8. Latimeria chalumnae. Cartilage histology (after SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of FRANCILLON et al., 1975). A, MECKEL’s cartilage (thin revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). histological section; Hemalun-PIC staining). An erosive periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells vascular cavity (black asterisk) is separated from the 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the medullary cavity (mc) by a layer of enchondral bone (eb). SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the Elongate chondrocytes (arrow-heads) are seen in the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific cartilage. (scale = 50 µm). B, Scapulocoracoid (ground as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and section 3 mm thick; x-ray). The cartilage (ca) is invaded by fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. resorption canals (white asterisks), their wall is covered by In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement thin bony layers, here clearly visible in white colour. The series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The white arrow-heads point to the erosion front of the cartilage. at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a (scale = 1 mm). C, Scapulocoracoid (thin histological half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is section; Stoelzner staining). In the cartilage (ca), the present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the vascular cavities (vc), resulting from a chondroclastic (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its activity, are bordered by thin bony lamellae here visible characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., in black colour (arrow-heads). (scale = 250 µm). These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 44 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 45 elements and eventually minute superficial endochondral 2008). 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This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of Fig. 9. Latimeria chalumnae. Lung plates. A, Isolated lung plate of an adult specimen (CCC24). (scale = 500 µm). B, Cross section between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral (azocarmin staining) in the anterior part of the vestigial lung showing its lumen (lu), two thin lung diverticles (arrows) and represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This four surrounding plates (1–4) (oe = ventral wall of the oesophagous). (scale = 1 mm). C, Detail of the lung plate n°3 of B, mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral showing the central weakness zone (*) and SHARPEY’s fibres (s) that enter the plate. (scale = 50 µm). D, Detail of a section 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). (hematoxylin-Eosin staining) in a lung plate showing an osteocyte lacuna (*) and the Liesegang lines (arrow-heads) that both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues characterize a spheritic mineralization. (scale = 20 µm). E, Detail (hematoxylin-Eosin staining) of two osteocyte lacunae (*) mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are with their osteocytic processes (arrow-heads) that penetrate the extracellular collagenous matrix. (scale = 20 µm). (B after as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in MILLOT and ANTHONY, 1978; C, D after CUPELLO et al., 2017). questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil Fig. 10. Latimeria chalumnae. Various odontodes. Ground CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The sections in A) the posterior field (= free ornamented area) ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous of a scale and B, C) a dermal bone. A, Odontode lying on adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of the external layer. Spheritic mineralized granules are seen This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil (arrow-heads) at the frontier of the external layer and the on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these first layers of the basal plate. B, Odontode lying at the at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large surface of a dermal bone. C, Dermal bone overlaid by the to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., dermis (white asterisks). Two odontodes are visible: one comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates at the surface of the bone with its tip eroded (arrow-heads), financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO and an older one (*) covered by more recent bony layers. de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (scale for A, B, C = 100 µm). (bp = basal plate; bo = bone; (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their de = dentine; pc = pulp cavity; vc = vascular cavity). EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 44 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 45 elements and eventually minute superficial endochondral 2008). 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Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of Fig. 9. Latimeria chalumnae. Lung plates. A, Isolated lung plate of an adult specimen (CCC24). (scale = 500 µm). B, Cross section between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral (azocarmin staining) in the anterior part of the vestigial lung showing its lumen (lu), two thin lung diverticles (arrows) and represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This four surrounding plates (1–4) (oe = ventral wall of the oesophagous). (scale = 1 mm). C, Detail of the lung plate n°3 of B, mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral showing the central weakness zone (*) and SHARPEY’s fibres (s) that enter the plate. (scale = 50 µm). D, Detail of a section 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). (hematoxylin-Eosin staining) in a lung plate showing an osteocyte lacuna (*) and the Liesegang lines (arrow-heads) that both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues characterize a spheritic mineralization. (scale = 20 µm). E, Detail (hematoxylin-Eosin staining) of two osteocyte lacunae (*) mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are with their osteocytic processes (arrow-heads) that penetrate the extracellular collagenous matrix. (scale = 20 µm). (B after as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in MILLOT and ANTHONY, 1978; C, D after CUPELLO et al., 2017). questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil Fig. 10. Latimeria chalumnae. Various odontodes. Ground CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The sections in A) the posterior field (= free ornamented area) ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous of a scale and B, C) a dermal bone. A, Odontode lying on adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of the external layer. Spheritic mineralized granules are seen This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil (arrow-heads) at the frontier of the external layer and the on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these first layers of the basal plate. B, Odontode lying at the at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large surface of a dermal bone. C, Dermal bone overlaid by the to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., dermis (white asterisks). Two odontodes are visible: one comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates at the surface of the bone with its tip eroded (arrow-heads), financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO and an older one (*) covered by more recent bony layers. de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (scale for A, B, C = 100 µm). (bp = basal plate; bo = bone; (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their de = dentine; pc = pulp cavity; vc = vascular cavity). EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 46 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 47 elements and eventually minute superficial endochondral 2008). 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Nature, 395: croissance du cœlacanthe Latimeria chalumnae SMITH, Elasmobranchs. 1: The endoskeleton, with remarks on the chalumnae (Pisces: Actinistia): a scanning electron ZYLBERBERG, L. and MEUNIER, F. J. 2008. New data on the discrete neural and haemal arches develop in the anterior part is no pore-canal system so Latimeria’s scales are not cosmoid, CONCLUSION In: GREENWOOD, P. H., MILES, R. S. and PATTERSON, C. 335. 1939 (Poisson, Crossoptérygien, Coelacanthidé). Cybium, hard tissues of lower vertebrates in general. Arkiv för microscopic study. Journal of Zoology, 185: 355–369. structure and the chondrocyte populations of the haemal of the notochord (MILLOT and ANTHONY, 1958). The anterior contrary to most of palaeozoic sarcopterygian fishes. Due to (eds.), Interrelationships of Fishes, Acad. Press, London, ERDMANN, M. V., CALDWELL, R. L., JEWETT, S. L. and 2: 129–137. Zoologi, 2: 321–454, 8 pl. SMITH, M. M. 1979. Scanning electron microscopy of cartilage of abdominal vertebrae in the adult carp neural and haemal spines are relatively short but they the presence of an unmineralized stratified basal plate, the This overview of eighty years (1938–2018) of histological pp. 137–177. TJAKRAWIDJAJA, A. 1999. The second recorded living JANVIER, P. 1996. Early Vertebrates. Clarendon Press, Oxford, ØRVIG T. 1968. The dermal skeleton; general considerations. odontodes in the scales of coelacanth embryo, Latimeria Cyprinus carpio (Teleostei, Ostariophysii, Cyprinidae). progressively increase in length posteriorly. Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. and haemal spines are composed of perichondral bone However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., surrounding a cartilaginous core (Fig. 2). homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 46 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT The skeleton and the mineralized tissues of the living coelacanths 47 elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. Transactions of the Royal Society of South Africa, UYENO, T. and YABUMOTO, Y. 2007. Origin of extant composed of the notochord which is coated by an unmineralized basal plate, where spheritic mineralized granules are seen in al., 2015, 2019). AGASSIZ, L. 1833–44. 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Volume 4, CRC Press, Boca Raton, pp. 171–224. upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. 48 François J. MEUNIER, Camila CUPELLO and Gaël CLÉMENT Bull. Kitakyushu Mus. Nat. Hist. Hum. Hist., Ser. A, 17: 49–56, March 31, 2019 elements and eventually minute superficial endochondral 2008). The basal plate in both species is unmineralized (Fig. 7) evolution, but with an important reduction of the bony plates in REFERENCES L. 2014. Divergence in skeletal mass and bone anatomy of the teeth and tooth supporting tissues of MONDEJAR-FERNANDEZ, J. 2018. On cosmine: its origins, SMITH, J. L. B. 1940. A living coelacanth fish from South Biological Reviews, 44: 91–154. Field surveys on the Indonesian coelacanth, Latimeria menadoensis using remotely been described. The aim of this study is to clear their habitat Allometric growth in the extant coelacanth lung during capture of a coelacanth off Madagascar. South African ossification (CASTANET et al., 1975). The axial skeleton is excepted at the contact between the superficial layer and the Latimeria linked to the vestigial state of its lung (CUPELLO et morphology in antarctic notothenioid fishes. Journal of Latimeria chalumnae. Archives of Oral Biology, 14: biology and implications for sarcopterygian Africa. 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Détermination de l’âge et ØRVIG T. 1951. Histologic studies of Placoderms and fossil SMITH, M. M. 1978. Enamel in the oral teeth of Latimeria Aquamarine Fukushima, pp. 24–26. DE VOS, L. and OYUGI, D. 2002. First capture of a coelacanth, A., HADIATY, R. and HADIE, W. 1999. A new species of vertebrae due to the lack of ossified centra, although some MEUNIER and ZYLBERBERG, 1999; MEUNIER et al., 2008). There ANDREWS, S. M. 1973. Interrelationships of crossopterygians. Indonesian “king of the sea” discovered. Nature, 395: croissance du cœlacanthe Latimeria chalumnae SMITH, Elasmobranchs. 1: The endoskeleton, with remarks on the chalumnae (Pisces: Actinistia): a scanning electron ZYLBERBERG, L. and MEUNIER, F. J. 2008. New data on the Masamitsu IWATA 1, Yoshitaka YABUMOTO2, Toshiro SARUWATARI3,4, Shinya YAMAUCHI1, Kenichi FUJII1, METHODS Latimeria chalumnae SMITH, 1939 (Pisces, Latimeriidae), coelacanth. Genetic and morphologic proof. C. 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Importantly neural scales of Latimeria are defined as elasmoid-like scales. work on Latimeria skeletal tissues allows some anatomical and BERNHAUSER, A. 1961. Zur Knochen- und Zah, histology von coelacanth from north Sulawesi. Environmental Biology 393 pp. In: ØRVIG T. (ed.), Current problems of lower vertebrate chalumnae SMITH. Archives of Oral Biology, 24: 179–183. Cybium, 32: 225–239. replaced with the second one in 2007. Our ROVs are able to overhang off Talise Island between 144 and 150 m deep. There again in October 2015 on a steep slope (Table 2: E25, E27). FRICKE, H., REINICKE, O., HOFER, H. and NACHTIGALL, W. SMITH, J. L. B. 1953. The second coelacanth. Nature, 171: and haemal spines are composed of perichondral bone However the plywood-like organization is considered to be evolutionary considerations. It can be enlightened a drastic Latimeria chalumnae Smith und einiger Fossilformen. of Fishes, 34: 445–451. MEUNIER, F. J. 1979. Etude histologique et microradiographique phylogeny. Proceedings of the fourth Nobel Symposium, SMITH, M. M., HOBDELL, M. H. and MILLER, W. A. 1972. The ZYLBERBERG, L., GÉRAUDIE, J., MEUNIER, F. J., & SIRE J. Y., 1Aquamarine Fukushima, Marine Science Museum, 50 Tatsumi-cho, Onahama, Iwaki, Fukushima, 971-8101, Japan dive up to 300 m depth. These had two vertical, two horizontal was almost no water current in this area. All individuals were The coelacanth ID 28 was found on the 1st November along 1987. Locomotion of the coelacanth Latimeria chalumnae 99–101. surrounding a cartilaginous core (Fig. 2). homologous with the bony basal plate of cosmoid scales of reduction of endochondral ossification during the long Sber. öst. Akad. Wiss., 170: 119–137. FAURÉ-FREMIET, M. 1936. La structure des fibres d’éastoidine. du cartilage hémal de la vertèbre de la carpe, Cyprinus Stockholm, 1967, J. Wiley, New-York. pp. 373–397. structure of the scales of Latimeria chalumnae. Journal of 1992. Biomineralization in the integumental skeleton of 2Kitakyushu Museum of Natural History and Human History, 2-4-1 Higashida, Yahata Higashi-ku, Kitakyushu, Fukuoka, and two right-left propellers and these were controlled from a close to each other under the same overhang and most of them one of the large rocks scattered on a gentle slope in a bay of in its natural environment. Nature, 329: 331–333. SMITH, C. L., RAND, C. S., SCHAEFFER, B. and ATZ, J. W. 1975. The scales belong to the exoskeleton. In both extant extinct sarcopterygian fishes (MEUNIER, 1980; SIRE and evolutionary history of coelacanths. The persistence of large BJERRING, H. C. 1973. Relationships of coelacanthiforms. In: Archives d'Anatomie Microscopique, 32: 249–269. carpio L. (Pisces, Teleostei, Cyprinidae). Acta Zoologica, PARMENTIER, E., COMPÈRE, P., CASADEWALL, M., FONTENELLE, Zoology, London, 167: 501–509. the living lower Vertebrates. In: HALL, B. K. (ed), Bone, 805-0071, Japan boat on surface through a 400 m long tether cable. The stayed still with their head facing downward. Four days later, the Lolak Island by 125 m depth. FRICKE, H., HISSMANN, K., SCHAUER, J., REINICKE, O., KASANG, Latimeria, the living coelacanth, is ovoviviparous. Science, 3 coelacanth species they are of elasmoid type, composed of an HUYSSEUNE, 2003; MONDEJAR, 2018; SCHULTZE, 2018). volume of cartilage in the endoskeleton at adult stage can be GREENWOOD P. H., MILES R. S. and PATTERSON C. (eds.), FOREY, P. L.- 1984. The coelacanth as a living fossil. In: 60: 19–31. N., CLOOTS, R. and HENRIST, C. 2008. The rocker bone: a THOMSON, K. S. 1969. The biology of the lobe-finned fishes. Volume 4, CRC Press, Boca Raton, pp. 171–224. Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashimanohara, Kashiwa-shi, Chiba, 277-8564, Japan underwater operations were visualized on a screen with ID 9 was observed again, alone on a steep slope at 172.9 m The encountered Indonesian coelacanths during these L. and PLANTE, R. 1991. Habitat and population size of 190: 1105–1106. 4Seikei Education and Research Center for Sustainable Development, Seikei Gakuen, 3-3-1 Kichijoji-Kitamachi, upper external layer also called “external ornamented layer”, Cartilages compared to the “little bone and considerable cartilage” that Interrelationships of Fishes, Acad. Press, London, pp. ELREDGE N. and STANLEY S.M. (eds.), Living fossils. MEUNIER, F. J. 1980. Les relations isopédine-tissu osseux dans new kind of mineralized tissue? Cell and Tissue Research, information including directions of ROVs, depth, water depth (Table 2: E12), which was located within several dozen surveys were in caves, alongside large rocks, under overhangs coelacanth Latimeria chalumnae at Grand Comoro. VENTER, P., TIMM, P., GUNN, G., LE ROUX, E., SERFONTEIN, E., Musashino-shi, Tokyo, 180-8633, Japan and of a lower thicker layer, called the basal plate, which is The cartilaginous tissues in Latimeria are characterized characterize the skeleton of a number of demersal notothenioid 179–205. Springer Verlag, Berlin, pp. 166–169. le post-temporal et les écailles de la ligne latérale de 334: 67–79. 5Research Center for Oceanography, Indonesian Institute of Science, Jl. Pasir Putih I, Ancol Timur, Jakarta, 14430, Indonesia temperature, date and time. All data were directly recorded on meters far from Talise-2 and 30 m deeper. or on steep slopes (Table 2; Fig. 2). Environmental Biology of Fishes, 32: 287–300. SMITH, P., SMITH, E., BENSCH, M., HARDING, D. and stratified and almost totally unmineralized (Fig. 3). The upper by long chondrocytes (Fig. 8) contrary to those of teleostean telostean fishes (EASTMAN et al., 2014). BRITO, P. M., MEUNIER, F. J., CLÉMENT, G. and GEFFARD-KURIYAMA, FOREY, P. L.- 1998. History of the Coelacanth Fishes. Latimeria chalumnae (SMITH). Zoologica Scripta, 9: PEGUETA, V. P. 1968. Enchondral ossification in Latimeria 6Technical Implementation Unit Marine Biota Conservation Bitung, Indonesian Institute of Sciences, Jl. Colombo, Kec, Maesa, video-tapes on the boat. Since the 2007 survey, water Four new coelacanths were recorded from the 29th Most individuals were found under overhangs or FRICKE, H., HISSMANN, K., SCHAUER, J., ERDMANN, M., HEEMSTRA, P. 2000. Discovery of a viable population of external layer is ornamented with radial crests. In the posterior fishes that are relatively spherical in shape (MEUNIER, 1979; A processus of spheritic mineralization has been recently D. 2010. The histological structure of the calcified lung Chapman and Hall, London, 419 pp. 307–317. chalumnae SMITH. Dopovidi Akademii Nauk Ukrainia Bitung Tengah, Maesa, Kota Bitung, Sulawesi Utara, 95511, Indonesia temperature and depth were independently recorded with more September to the 6th October 2009 in Talise and Banggka alongside large rocks. Some individuals were encountered not MOOSA, M. K. and PLANTE, R. 2000. Biogeography of the coelacanths (Latimeria chalumnae SMITH, 1939) at 7 area of the scale these radial reliefs are overlain by numerous ZYLBERBERG and MEUNIER, 2008). Cartilage tissues can show highlighted in various skeletal elements of Latimeria, by the of the fossil coelacanth Axelrodichthys araripensis FRANCILLON, H., MEUNIER, F., NGO TUAN PHONG, D. and MEUNIER, F. J. and ZYLBERBERG, L. 1999. The structure of the SSR., 7: 653–656 (in Russian; English abstr.). Research Center for Deep Sea, Indonesian Institute of Science, Jl. Y. Syaranamual, Guru-Guru, Poka, Ambon, 97233, Indonesia accuracy by external measuring memories (Alec Electronics, Islands and off Manado (Table 2: E13 and 14, ID 13, 14, 15). to hide in any shade and stayed just on rocky slopes. In Indonesian coelacanth. Nature, 403: 38. Sodwana Bay, South Africa. South African Journal of 8 denticulations, the odontodes, which can be superposed (Fig. an endochondral ossification process. This phenomenon has presence of globular dentine in teeth, in odontodes of the (Actinistia: Mawsoniidae). Palaeontology, 53: 1281–1290. RICQLÈS, A. (DE). 1975. Données préliminaires sur les external layer and of the odontodes of scales in Latimeria POUYAUD, L., WIRJOATMODIO, S., RACHMATIKA, L., Faculty of Fisheries and Marine Science, Sam Ratulangi University, Jl. Kampus UNSRAT Bahu, Manado, Sulawesi Utara, later named JFE Alec; MDS-MKV/T, MDS-MKV/D). In ID 15 is the only juvenile coelacanth filmed so far. It was in a overhangs and cracks, all individuals had their ventral side HEEMSTRA, P. C., FREEMAN, A. L., WONG, H. Y., HENSLEY, D. Science, 96: 567–568. 95115, Indonesia 3). The anterior area of the external layer, which is covered by been studied respectively on the urohyal (PEGUETA, 1968), the tegumentary skeleton (scales, fin rays), in scales at the interface CASANE, D. and LAURENTI, P. 2013. Why coelacanths are structures histologiques du squelette de Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) TJAKRAWIDJAJA, A., HADIATY, R. K. and HADIE, W. 1999. addition two laser beam irradiators, that provide line lasers of small crack between 164.6 and 170.9 m deep in a temperature alongside and close to a rock wall, but without touching it. A. and RABESANDRATANA, H. D. 1996. First authentic the anterior scales, shows crests with irregularities that have MECKEL’s cartilage and the proximal piece of the pectoral between the external layer and the basal plate, as well as in not ‘living fossils’. Bioessays, 35: 332–338. DOI chalumnae. I I- Tissus osseux et cartilages. In: Coll. Inter. revisited using scanning and transmission electron Une nouvelle espèce de coelacanthe, preuves génétiques 20-cm distance, were attached to the second ROV and have between 14.5 and 15 °C. Estimated total lengths are shown in Table 3. Most been interpreted as growth marks and tentatively used for girdle (FRANCILLON et al., 1975). The endochondral ossification lung bony plates. The spheritic mineralization (i.e., a radiating 10.1002/bies.201200145. CNRS, "Problèmes actuels de Paléontologie. Evolution microscopy. In: SÉRET, B. and SIRE, J.-Y. (eds.), Proc. 5th et morphologiques. Comptes Rendus de l’Académie des (Received August 24, 2018; accepted November 9, 2018) been used to register the size of encountered animals. The The shallowest record of a coelacanth was at 115.6 m individuals are more than 1 m in total length. ID 15 is a ageing coelacanths (HUREAU and OZOUF, 1977; MILLER, 1979). is relatively limited when it occurs and the volume of enchondral arrangement of hydroxyapatite crystals and of the organic CASTANET, J., MEUNIER, F., BERGOT, C. and FRANÇOIS, Y. des Vertébrés", Paris, 4–9 Juin 1973, Centre National de Indo-Pacific Fish Conf., Nouméa, 1997, Soc. Fr. Ichtyol., Sciences, 322: 261–267. surveys were conducted off northern parts of Sulawesi Island depth off the southern part of Manado (Table 2: E16, juvenile individual of 31.5 cm and ID 23 is 90 cm in total The tooth plates of the buccal cavity support series of bone remains reduced to thin bony layers (Fig. 8). The cartilage matrix) in vertebrate skeletal tissues is considered as a 1975. Données préliminaires sur les structures la Recherche Scientifique, pp. 169–174, 2 pls. Paris, pp. 109–116. ROMER, A.S. 1937. The braincase of the carboniferous and along the Biak Island located in northwestern New Guinea Manado-3) on the 9th October in 2009. ID 16 (Table 2) was length. No individual beyond 140 cm has been recorded in teeth of various sizes (Fig. 4). They range in three morphotypes: is destroyed by chondroclasts in areas where endochondral precursor of inotropic mineralization (specific interactions histologiques du squelette de Latimeria chalumnae. I - FRANCILLON-VIEILLOT H., BUFFRENIL V. DE, CASTANET J., MEUNIER, F. J., ERDMANN, M. V., FERMON, Y. and CALDWELL, crossopterygian Megalichthys nitidus. Bulletin of the ABSTRACT − Habitats of the Indonesian coelacanth, Latimeria menadoensis, were investigated by Remotely Island, Indonesia. The areas and time periods of each survey found at the end of the morning, alone alongside a large rock Indonesia so far. restricted as those of the African coelacanths, and so a broader and other staffs for our work on the research boat. Dr. BATUNA Operated Vehicles (ROVs) surveys in the northern coast of Sulawesi Island and southern coast of Biak Island by the fangs (7–10 mm in height), middle-sized teeth (3–4 mm in ossification occurs. Serial chondrocytes, known at the origin of between collagen fibrils and the mineral phase) that possibly Dents, écailles, rayons de nageoires. In: Coll. Inter. GÉRAUDIE J., MEUNIER FJ., SIRE J-Y., ZYLBERBERG L., R. L. 2008. Can the comparative study of the morphology Museum of Comparative Zoology, 824: 1–73. are shown in Table 1 and Fig. 1. on the edge of a shelf. The water temperature was about 20.0 distribution of the Indonesian coelacanth could be expected. and the Murex staffs supported our daily life during the collaboration of Aquamarine Fukushima (Japan), and Indonesian Institute of Sciences and Sam Ratulangi INTRODUCTION Since the discovery of the Raja Laut (“king of the sea”), height) and rounded tubercles (MILLOT and ANTHONY, 1958). the calcified cartilage, seem to be lacking in the endochondral represents a derived evolutionary stage of calcification CNRS, "Problèmes actuels de Paléontologie. Evolution and RICQLÈS A. DE 1990. Microstructure and and histology of the scales of Latimeria menadoensis and ROMER, A.S. 1942. Cartilage as an embryonic adaptation. ºC. Occurrences of coelacanths along the eastern coast of the expeditions. We would like to express our sincere thanks to off Sulawesi Island in Indonesia (ERDMANN et al., 1998, 1999), The teeth of the two first categories are conical and sharp ossification process in Latimeria (FRANCILLON et al., 1975). This mechanisms (ØRVIG, 1951, 1968; FRANCILLON-VIEILLOT et al., des Vertébrés", Paris, 4–9 Juin 1973, 159–168, 4 Pls. mineralization of vertebrate skeletal tissues. In: CARTER, L. chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) American Naturalist, 76: 394–404. University (Indonesia) from 2005 to 2015. The Remotely Operated Vehicles operations were conducted 1173 From the 6th to the 16th November in 2010, the field of the propellers of the ROV. level changed, the water flow was reversed. Coelacanths African continent were recorded in South Africa (SMITH, colleagues at Aquamarine Fukushima, Japan, for their times and coelacanths were encountered 30 times. A total of 30 different individuals were observed at a depth range The first study of fossil coelacanths was done by AGASSIZ the genus Latimeria comprises two species: L. chalumnae SMITH whereas those of the third category have an obtuse tip (Fig. 5). constitutes a true difference with teleostean endochondral 1990; ZYLBERBERG et al., 1992). The simultaneous presence of CLEMENT, G. 1999. The actinistian (Sarcopterygii) Piveteauia J. G. (ed.), Skeletal Biomineralization: Patterns, bring new insight on the taxonomy and the biogeography ROUX, G. H. 1942. The microscopic anatomy of the Latimeria RESULTS survey was conducted around Biak Island (Table 1: R9). Adult DISCUSSION Temperature and depth data for each Indonesian always kept their head against the water flow, like other 1939), Comoros (SMITH, 1953), Madagascar (HEEMSTRA et al., understanding and supports. We would like to thank Dr. Gaël (1833–44) and was followed by a lot of papers with the 1939 and L. menadoensis POUYAUD et al., 1999. However our Fangs of Latimeria are inserted into a socket (MILLOT and the bony plates of fossil and extant coelacanths (BRITO et al., ossifications (MEUNIER, 1979; ZYLBERBERG and MEUNIER, 2008). both mineralization processes (spheritic and inotropic) in the madagascarensis LEHMAN from the Lower Triassic of Processes and Evolutionary Trends. Vol. I, Van of recent coelacanthids? Geological Society, London, scale. South African Journal of Medical Sciences, 7: 1–18. from 115.6 m to 218.9 m deep. The water temperature was between 12.4 to 21.5 ºC. Most of the individuals were coelacanths were found at two different sites (Table 2: coelacanth record are shown in Fig. 3. Though an average of observed actinopterygian fishes did. It means that as the 1996), Kenya (DE VOS and OYUGI, 2002), Tanzania (BENNO et CLÉMENT of Muséum national d’Histoire naturelle and Dr. discovery of new fossils (see reviews of JANVIER, 1996 and knowledge of the anatomy and biology of the living coelacanths ANTHONY, 1958; HOBDELL and MILER, 1969; CASTANET et al., 2010; CUPELLO et al., 2017). Tooth tissues mineralized tissues of Latimeria and in other osteichthyans such Northeastern Madagascar: a redescription on the basis of Nostrand, New York, pp. 471–530 Special Publications, 295: 351–360. SASAGAWA, I., ISHIYAMA, M. and KODERA, H. 1984. Fine found alone, however, schools of two, three and six individuals were also observed. The Indonesian coelacanth, L. The field survey of the Indonesian coelacanth, Latimeria E17–19). Two individuals (ID 17 and 18) were found under an During the field surveys by underwater ROV recording water temperature on the ocean surface was about 30 °C, the direction of the water flow changed, the swimming direction of al., 2006), and Mozambique (BRUTON et al., 1992). In Camila CUPELLO of Universidade do Estado do Rio de Janeiro FOREY, 1998). Fossil coelacanths constitute an important is so far essentially based on L. chalumnae. 1975) and they have a smooth external surface (MILLOT et al., The three tooth morphotypes described in Latimeria are as teleosteans (ZYLBERBERG and MEUNIER, 2008) is however new material. Journal of Vertebrate Paleontology, 19: GARRAULT, H., 1936. Développement des fibres d’élastoidine MEUNIER, F. J., BRITO, P. M. and LEAL, M.-E. 2013. Quelques structure of the pharyngeal teeth in the coelacanth fish menadoensis, was observed at a similar depth of the African coelacanth, Latimeria chalumnae, and the temperature menadoensis, was conducted 14 times from 2005 to 2015 with overhang between 212.5 and 218.9 m deep (Table 2: Biak-1) for Indonesian coelacanths, Latimeria menadoensis, from 2005 temperature often dropped into about 11 °C at 300 m water depth. each coelacanth individual changed accordingly. Indonesia, coelacanths have only been found off the northern as a referee for their critical reading of the manuscript and their monophyletic group composed of more than forty genera, 1978; MEUNIER et al., 2015). fangs (7–10 mm in height), middle-sized teeth (3–4 mm in questionable. The mineralized spherules present at the limit 234–242. (actinotrichia) chez les salmonides. Archives d'Anatomie données morphologiques et histologiques sur la structure (Latimeria chalumnae). In: FEARNHEAD, R. W. and SUGA, range also seems to be very similar. However, Latimeria menadoensis was sometimes observed besides big rocks 1173 underwater operations around Sulawesi and Biak islands on the 11th November. Three other ones (ID 19, 20, 21) were to 2015, 30 different individuals were identified and three The temperatures changed widely even though the changes of On the 24th September 2009 (Table 2: E11) six coast of the Sulawesi Island and the southern coast of the Biak comments. eighty species, and belong to the Sarcopterygii (ANDREWS, A particularity of the exoskeleton of Latimeria is the ADULT LATIMERIA SKELETAL TISSUES height) and rounded tubercles (MILLOT and ANTHONY, 1958). between the external layer and the basal plate of Latimeria CLEMENT, G. 2005. A new coelacanth (Actinistia, Microscopique, 130: 105–137. de la plaque dentaire linguale d’Arapaima gigas S. (eds.), Tooth enamel IV, Elsevier Science Publishers, or the steep wall. It seems to be less sensitive to daylight than L. chalumnae. Here we report also, for the first time in Indonesia (Fig. 1, Table 1). No coelacanth was encountered registered under an overhang between 193.2 and 195.9 m deep others were unidentified. Among those, six individuals were depth were small at several places. All Indonesian coelacanths, individuals were recognized under an overhang (Talise-2). The Island in northern New Guinea. Unfortunately one of our authors, Dr. Djoko Hadi KUNARSO 1973; JANVIER, 1996; FOREY, 1998; UYENO and YABUMOTO, THE LATIMERIA SKELETON abundance of odontodes at the surface of various skull bones These teeth and tubercles are constituted of a cone of scales are considered to be the product of an inotropic Sarcopterygii) from the Jurassic of France, and the GÉRAUDIE, J. and MEUNIER, F. J. 1980. Elastoidin actinotrichia (Osteoglossidae; Teleostei). Cybium, 37: 263–271 Amsterdam, pp. 462–466. in the world, a juvenile coelacanth was observed in a small crack at 165 to 171 m depth during these surveys. during the first surveys in 2005 although 452 underwater (Table 2: Biak-2) on the 13th November. Two days later, observed more than twice: ID 3 at Buol-2, 3, 5, 6 (Table 2: E3, L. menadoensis, were encountered during day time at a depth all had about the same size. There was almost no water flow, Field surveys of the Indonesian coelacanths should be has passed away during the process of this contribution. We 2007; and many others). For a century coelacanths were Bony tissues SHARPEY’s fibres and/or growth marks (Fig. 6). regarded as a plesiomorphic character for Osteichthyes orthodentine set around a large pulp cavity and overlain by an type according to the definition of MEUNIER et al. (2013). This present on the surface of the plates, and conjunctive fibres mineralization (MEUNIER and ZYLBERBERG, 1999). It thus question of the closest relative fossil to Latimeria. in coelacanth fins: a comparative study with teleosts. MEUNIER, F. J., MONDEJAR-FERNANDEZ, J., GOUSSARD, F., SCHULTZE, H.-P. 1969. Die Faltenzähne der Rhipidistiden operations were conducted around Manado-tua Island and spots pattern on its body, an ID number was allocated. The temperature changed up and down by five degrees during the between the maximum and the minimum was 6.7 °C, which Biak-2 was observed again and only ID 20 stayed there. E4, E6 and E7); ID 8 at Talise-1 (E9 and E10), ID 9 at Talise 2 between 115.6 and 218.9 m and a temperature between 12.4 and each individual was head downward. They were close to continued in all area of Indonesia and expanded to all pray for the response of his soul. considered extinct since the end of the Cretaceous time (Fig. 1). The first anatomical observations on the extant coelacanth Cortical areas of the dermal skeleton are constituted of The dermal fin rays that sustain paired and unpaired fins (GÉRAUDIE and MEUNIER, 1980, 1984). external hypermineralized layer considered as true enamel organization is less complex than the three other plicidentine (SHARPEY’s fibres) penetrate within the plate (Fig. 9C). The appears that the state of the mineralized spherules observed in Journal of Vertebrate Paleontology, 25: 481–491. Tissue and Cell, 12: 637–645. CLÉMENT, G. and HERBIN, M. 2015. Presence of plicidentine Crossopterygier, der Tetrapoden und der Actinopterygi- KEY WORDS: Indonesian coelacanth, underwater survey, Latimeria menadoensis, Sulawesi, Biak, ROV other close Indonesian islands from the 17th to 30th of April individual which could not be distinguished was allocated an observation due to water flow reversals. When the water flow was the largest range of all surveys. Two new coelacanths were recorded off Manado in and 3 (E11 and E12), ID 20 at Biak-2 (E18 and E19), ID 24 at and 21.5 ºC. Indonesian coelacanths have exceptionally been each other but no direct contacts or interactions between Southeast Asia in order to increase our knowledge of the This study was supported in part by funding from With the discovery of a living coelacanth in 1938 (SMITH, were done by SMITH (1940). The anatomy of the Latimeria primary periosteal bony tissue. Its mineralization is in Latimeria are true lepidotrichia (CASTANET et al., 1975). The upper layer of the Latimeria scale is relatively thin (GRADY, 1970; CASTANET et al., 1975; SHELLIS and POOLE, 1978; types (polyplocodont, eusthenodont and dendrodont), which extracellular matrix shows various staining intensities with the various skeletal tissues of Latimeria, including the lung CUPELLO, C., BRITO, P. M., MEUNIER, F. J., HERBIN, M., GÉRAUDIE, J. and MEUNIER, F. J. 1984. Structure and in the oral teeth of Latimeria chalumnae (Sarcopterygii; er-Gattung Lepisosteus nebst einer Beschreibung der survey. (Table 1, R1). The second field survey was held along the UN (unknown) + number. was reversed some times, all individuals always changed their On the next day, on the 15th December, the ID 3 was December 2010 (Table 1: R10; Table 2: E 20 and 21; ID 22 Manado-6 and 8 (E22 and E24), ID 26 at Lolak-1 and 3 (E25 recorded in an environment with a temperature exceeding 20 coelacanths were observed. No evidence of a social behavior distribution of this rare species and to define, in a close future, Interdisciplinary Collaborative Research program of Atmosphere 1939) the scientific community was soon highly interested to skeleton has been later described in detail by MILLOT and heterogeneous and generally marked by series of growth lines, They are made of two parallel opposite gutter-shaped and it is constituted of bony tissue with embedded osteocytes, SMITH, 1978; SASAGAWA et al., 1984). Various studies have are described in most of extinct and extant Sarcopterygii concentric and parallel (Fig. 9D) or globular shaped lines. bony plates, must be studied with adapted ultrastructural JANVIER, P., DUTEL, H. & CLÉMENT, G. 2015. Allometric comparative morphology of camptotrichia of lungfish Actinistia; Coelacanthidae). Journal of Structural Biology, Zahnstruktur von Onychodus (Struniiformer Crossoptery- northern coast of Sulawesi from the 6th to 19th May in 2006, In the end of the morning of the same day, a third directions against the water flow. observed again under an overhang (Table 2: E7, Buol-6) near and 23). and E27). ID 8 was observed on the 14th September 2009 and ºC, regardless of the depth. The African coelacanth, L. has been recognized in the Comorian populations of the most relevant conservation policies of the different known and Ocean Research Institute, the University of Tokyo. compare the incomplete fossil sarcopterygian fishes dataset to ANTHONY (1958). The living coelacanth shows a general probably due to alternative physiological cycles linked to hemirays, each of which being a series of hemisegments whereas the basal plate is much thicker and composed of revealed the presence of globular dentine (Fig. 5) at the (SCHULTZE, 1969, 1970). These lines are considered to be Liesegang lines that characterize techniques in order to test their true origin: spheritic or growth in the extant coelacanth lung during ontogenetic fins. Tissue and Cell, 16: 217–236. 190: 31–37. gier). Palaeontologica Italica, New Series, 35(65): 63–137. but once again despite of 107 underwater operations no individual (Table 2: E3, ID 3) was found in another cave During the field survey carried on December of the same other sites where it was previously found at Buol-2 , Buol-3 On the 4th May 2012, an individual (Table 2: E22, ID 24) was encountered again at the same place (Talise-1) the day chalumnae, was observed by submarine vehicles in steep coelacanths (FRICKE et al., 1991). populations. the recent anatomical and biological organization of Latimeria organization similar to that of the other actinistian fishes seasonal variations (Fig. 6). The cortical primary bone shows articulated by a collagenous ligament. Each hemisegment is numerous strata made of thick collagenous fibres (Fig. 7). periphery of the first third of the tooth (MILLER and HOBDELL, The bony plates of the lung an active spheritic mineralizing process. The lung plates of inotropic mineralization? development. Nature Communications, 6: 8222. DOI: GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, MILLER, W. A. 1979. Observations on the structure of SCHULTZE, H.-P. 1970. Folded teeth and the monophyletic coelacanth was recorded. (Buol-2), larger and located 20 m deeper (Buol-2) than the first year, in the same Buol area (Table 1: R4) the sixth individual and Buol-5. Its posture was upside down with its ventral side was found on a steep slope at 169.4 m depth off Manado after. ID 24 was observed on the 4th May 2012 and then 13 slopes between 150 m and 253 m (FRICKE et al., 1991). Divers According to the observations of the African coelacanths, chalumnae. Many authors (see THOMSON, 1969; MILLOT and (THOMSON, 1969; JANVIER, 1996; FOREY, 1998). The skeleton (MILLOT and ANTHONY, 1958; BERNHAUSER, 1961), on the fin SMITH, 1978; SASAGAWA et al., 1984; MEUNIER et al., 2015). vascular canals and numerous SHARPEY’s fibres (Fig. 6B). The made of a mineralized collagenous fibrillary matrix with Between two collagenous layers there are star-shaped cells 1968; HOBDELL and MILLER, 1969; SHELLIS and POOLE, 1978; The lung of Latimeria is reduced to a short oesophagus Latimeria are thus true bony plates, and are homologous with the 10.1038/ncomms9222. Y. 1978a. The fibrous structure of coelacanth scales: a mineralized tissue of the coelacanth, including scales and origin of Tetrapods. American Museum Novitates, 2408: INTRODUCTION of the reproduction biology of the coelacanths is almost The first individual of Indonesian coelacanth (Table 2, ID cave (Buol-1). After 29 minutes of recording, this individual (Table 2: E5, ID 6) was recognized at 14:34 on the 12th facing the ceiling of the overhang. Such posture is also known (Table 2: Manado-6). It swam up and down 5.4 m between months later, on the 9th June 2013 at the same locations of recorded the presence of this species at 104 m depth at the species L. chalumnae is nocturnal and hides in cave in REFERENCES ANTHONY, 1958; MILLOT et al., 1978 FOREY, 1984, 1998; can be divided in various parts (Fig. 2): skull, axial skeleton, rays (CASTANET et al., 1975) and on the posterior (free) area of Contrary to the superficial skeleton, there are clearly less centre of these bones is frequently made of a spongiosa with embedded osteocytes. The hemisegments are sometimes fused (SMITH et al., 1972, pl. VI; CASTANET et al., 1975, fig. 12), the SASAGAWA et al., 1984). This typical histological organization diverticulum (CUPELLO et al., 2015) surrounded by scattered large bony plates known in the abdominal cavity of fossil CUPELLO, C., CLEMÉNT, G., MEUNIER, F. J., HERBIN, M., twisted "plywood". Tissue and Cell, 10: 671–686. their associate odontodes. Occasional Papers of the 1–10. restricted to an ovoviviparity strategy since some caught large 1) was recorded during the third field survey, in the morning of hid inside the cave. Although the water temperature increased December alongside a large rock. This individual stayed in the in coelacanths from the Comorian Archipelago (FRICKE et al., 168.1 and 173.5 m deep for 17 minutes. Thirteen months later Manado area within several kilometers. Sodwana Bay, South Africa (VENTER et al., 2000). Latimeria daytime but comes out at night, supposedly in search of food ACKNOWLEDGMENTS JANVIER, 1996) focused their work on Latimeria as a key-taxon paired and unpaired fins, tegumentary skeleton (scales). The scales (Fig. 3) (MILLOT and ANTHONY, 1958; CASTANET et al., histological studies of the skeletal bony elements (FRANCILLON vascular cavities surrounded by secondary bony deposits that at the basal part of the rays due to centrifugal deposition of elasmocytes, which cytoplasmic processes insert between the characterizes the various teeth of the bucco-pharyngeal cavity small and thin ovoid plates (Fig. 9A, B). These plates cover the actinistians (BRITO et al., 2010; CUPELLO et al., 2017). The ACKNOWLEDGEMENTS YABUMOTO, Y. and BRITO, P. M. 2019. The long-time GIRAUD, M. M., CASTANET, J., MEUNIER, F. J. and BOULIGAND, Californian Academy of Sciences, 134: 68–78. SCHULTZE, H.-P. 2018. Hard tissues in fish evolution: history The first living coelacanth, Latimeria chalumnae, was females carried unfertilized eggs or embryos in their oviduct the 30th May 2006 (Table 1, R3). The coelacanth was of more than five degrees, from 14.8 to 20.4 ºC, it stayed at the beginning of the observation and then moved ahead to deeper 1987). ID 3 was found totally four times in this area in two (the 9th June 2003), this individual (ID 24) was observed again All individuals observed more than twice were chalumnae seem to prefer a temperature range of 15–20 °C, (FRICKE et al., 1991). The living geomorphologic environment BENNO, B., VERHEIJI, E., STAPLEY, J., RUMISHA, C., NGATUNGA, to test or propose various hypotheses on the origin and skull, axial skeleton and fins are constituted of endoskeletal 1975; HADIATY and RACHNATIKA, 2003; MEUNIER et al., 2008). et al., 1975). Meanwhile, in addition to the usual skeletal result from remodelling processes (Fig. 6). This secondary bony laminae around the primary articulation, and eventually collagenous fibres. These fibres are set in a very specific as well as the various odontodes of the dermal bony plates, the surface of the vestigial lung, and are composed of a fibrous calcified walls that surrounded the lung of the Cretaceous adaptation of coelacanths to moderate deep water: Y. 1978b. Organisation spatiale de l'isopédine des écailles MILLER, W. A. and HOBDELL, M. H. 1968. Preliminary report and current issues. Cybium, 42(1): 29–39. discovered in South Africa in the Indian Ocean in 1938 (SMITH et al., 1975; CUPELLO et al., 2015). observed in a cave of 165 m depth (Table 2, Boul-1) for 10 same place, not moving away. Despite it disappeared from the slowly. Eventually it reached 12 m deeper during one hour and surveys during the seven months and seems to live in this area. near a cliff at 152.3 m depth (Table 2: E24, Manado-8), where encountered in the same area, at locations close from each where they tend to choose their daytime habitats (FRICKE et al., of L. menadoensis is similar to that of L. chalumnae, with We are grateful to Dr. Teruya UYENO for his valuable B., ABDALLAH, A. and KALOMBO, H. 2006. Coelacanth evolutionary history of the early tetrapods and sarcopterygii in elements that are overlain by exoskeletal elements. In the Among the various components of the whole skeleton, elements, specific bony tissues have been described in fossil bone is separated from the primary one by reversal cementing to the mineralization of the ligament (see figs. 19, 20 in network. In each layer, the fibres are parallel to each other and fin rays and the scales (CASTANET et al., 1975). matrix with fibrocytes: it is a cellular bony tissue (CUPELLO et coelacanth Axelrodichthys are made of large osseous plates of This contribution is linked to an international roundtable reviewing the evidences. Bulletin of Kitakyushu Museum du coelacanthe (Latimeria chalumnae SMITH). Comptes on the histology of the dental and paradental tissues of SHELLIS, R. P. and POOLE, D. F. G. 1978. The structure of the (SMITH, 1939). The first observation of the living coelacanth The Indonesian coelacanth, L. menadoensis, was first minutes (Table 2, E1). The adult individual was in stationary camera frame we kept setting the ROV there in front of the 42 minutes. During the 2007 survey (Table 1: R5) a coelacanth (Table located on the same slope of Manado-6. other within hundreds of meters. However, in the Comorian 1991). The suitable temperature for L. menadoensis seems to be rocky steep slopes with undermarine caves or overhangs. advice, guidance and encouragement throughout the present (Latimeria chalumnae SMITH, 1939) discoveries and general, and to infer their possible biological characteristics. extant Latimeria the endoskeleton of the skull shows an and apart the SMITH’s pioneer work (SMITH, 1940), numerous (BRITO et al., 2010) and extant coelacanths (CUPELLO et al., lines that are hypermineralized. CASTANET et al., 1975). Odontodes observed on the external the direction of the fibres change from a layer to another one. In the fang the inner wall of the pulp cavity displays a al., 2017). Each plate is enclosed in a membranous bag. These various thickness (BRITO et al., 2010), as those of other fossil on coelacanths evolution held at the Kitakyushu Museum and of Natural History and Human History Series A (Natural Rendus de l’Académie des Sciences, 287: 487–489. Latimeria chalumnae (SMITH) with a note on tooth dental hard tissues of the coelacanthid fish Latimeria habitats using submersibles was reported in Comoros (FRICKE discovered in Manado, Sulawesi Island, Indonesia, in 1997. position in a cave (Buol-1) slowly moving its pectoral, pelvic, cave until the next morning, however it did not appear again. On the 14th December, the individual ID 3 previously 2: ID 7) was recorded off Manado by 195 m depth, with a Another new coelacanth (Table 2: E23, ID 25) was Archipelago, same individuals of L. chalumnae were observed, almost the same as L. chalumnae. However, Latimeria menadoensis was also observed alongside study. Many thanks go to colleagues of the Faculty of Fisheries conservation in Tanzania. South African Journal of The fossil sarcopterygian fishes are known by their fossilized important regression of the bones, especially in the studies have been carried out on the histological organization 2015, 2017), such as the mineralized plates surrounding the Bone remodelling in adult specimens can be more or less convex surface of the rays are similar to those present on the This regular organization results in a spatial arrangement series of plies (Fig. 5; MEUNIER et al., 2015). These plies start plates look fragile in their middle plane since a central coelacanths (CLEMENT, 1999, 2005). The bony tissue of these at the Aquamarine Fukushima in August 2017. We would like History), 17: 29–35. GRADY, J. E. 1970. Tooth development in Latimeria replacement. Archives of Oral Biology, 13: 1289–1291. chalumnae SMITH. Archives of Oral Biology, 23: et al., 1987). Latimeria chalumnae hide in submarine caves The first specimen was captured in 1998 (ERDMANN et al., second dorsal and anal fins. The day after, another individual On the 4th June in 2006, three individuals, including ID 3 recorded at Buol-2 in a cave and at Buol-3 in a crack, was temperature of 12.4 °C, the coolest one registered during all recorded alone on a Manado site (Manado-7). within a two week period, in several caves distributed in a 8 Water temperature can increase or drop for more than 5 large rocks or along vertical wall in daytime. Some of these and Marine Sciences of the Sam Ratulangi University at Science, 102: 486–490. mineralized tissues, essentially their bones, scales and teeth. neurocranium, which are replaced by cartilaginous tissues, as of scales (ROUX, 1942; SMITH et al., 1972; CASTANET et al., lung. These bony plates in actinistians do not belong to the developed according to a bone and within a given bone. dermal bones of the skull and scales. The distal extremity of termed “twisted plywood” (GIRAUD et al., 1978a,b). The at the base of the tooth and reach at least the first third to the weakness zone opened on the microtome knife, creating an plates is a vascularized cellular bone with more or less large to thank the anonymous reviewers for their constructive CUPELLO, C., MEUNIER, F. J., HERBIN, M., JANVIER, P., chalumnae (SMITH). Journal of Morphology, 132: 377–388. MILLOT, J. and ANTHONY, J. 1958. Anatomie de Latimeria 1105–1113. along steep slopes between 100 m and 200 m depth during 1998). According to a genetic study, the specimen differed (ID 2) and an unidentified one (UN1) were found in the same which was observed on the 31th May at Buol-2 and two new encountered again (Table 2: Buol-5) near a vertical wall at 145 surveys. Field surveys were conducted from the 19th to 30th May kilometers wide area (FRICKE et al., 1991). °C in a very short period of time (about 30 min according to our individuals were encountered above 200 m deep, in an Manado, Indonesia, for their generous supports to conduct BRUTON, M. N., CABRAL, A. J. P. and FRICKE, H. 1992. First Together with the extant lungfishes, especially Neoceratodus, in its Mesozoic fossil actinistian relatives (ROMER, 1937, 1942; 1975; GIRAUD et al., 1978a; MILLER, 1979; SMITH, 1979; skeleton sensu stricto. They are specific bony specializations Primary bone is destroyed by osteoclasts and the deposition the lepidotrichia is overlapped by actinotrichia (GÉRAUDIE and rotation of fibres direction from one layer to the next has a half of the tooth towards its tip (Fig. 5). Such plies are also artefactual lumen (Fig. 9C) (CUPELLO et al., 2017). The fibres vascular cavities and some internal remodelling (BRITO et al., comments and valuable suggestions. C.C. was partially CLÉMENT, G. and BRITO, P. M. 2017. The homology and HADIATY, R. K. and RACHMATIKA, I. 2003. Morphological chalumnae. T. 1. Squelette, muscles et formations de SIRE, J.-Y. and HUYSSEUNE, A. 2003. Formation of dermal daytime and come out and drift near the ocean floor for from L. chalumnae and a new species was erected (POUYAUD cave (Buol-1). The unidentified one immediately hid deeper in individuals, were observed in a vertical crack which was m depth (Table 2: E6). After a while, this individual (ID 3) The field survey in 2009 was carried out off Manado and 2015 off Lolak Island and from the 30th October to the 16th When individuals of L. menadoensis were encountered, recordings). The coelacanths however often stayed there environment that remains slightly bright. Latimeria expeditions. Also we express our thanks to Dr. SUHARSONO, Dr. capture of a coelacanth, Latimeria chalumnae (Pisces, Latimeria offered a unique access to the skeleton as a whole: MILLOT and ANTHONY, 1958; BJERRING, 1973; FOREY, 1998). MEUNIER, 1980; MEUNIER and ZYLBERBERG, 1999; HADIATY in relation to the lung (see below), as is the “rocker bone” in process of the secondary bone results from the activity of MEUNIER, 1980) that are long tapered rods of elastoidin , a mean angle of 27° (GIRAUD et al., 1978a). This organization is present but less developed in the small caniniform teeth are collagenous and organized in superposed layers. The cells 2010). Moreover the mineralization of the lung ossified plates financed by the Coordenação de Aperfeiçoamento de Pessoal function of the lung plates in extant and fossil study of the scales of Latimeria menadoensis POUYAUD et soutien. CNRS Edr., Paris. 122 pp., 80 pls. skeletal and dental tissues in fish: a comparative and hunting prey at night (FRICKE et al., 1991). However, since the et al., 1999). In 1999 two individuals were observed by the cave, where the ROV could not access, and only its lateral several hundred meters far from Buol-2 (Buol-3) for 2 hours moved upward about 18 m and stayed behind a large rock (Fig. around Talise and Bangka islands off the northern coast of November 2015 off Lolak and Bitung Islands (Table 1; R13 some of them stayed stationary at same place but some without moving away or significantly modifying their menadoensis seems to be less sensitive to the daylight than L. Zainal ARIFIN, Dr. DIRHAMSYAH and colleagues of the Indonesian Latimeriidae), off Mozambique. South African Journal of with both mineralized and unmineralized skeletal tissues. Here, In the same way, the endoskeleton of paired and unpaired fins and RACHMATIKA, 2003; MEUNIER et al., 2008) and teeth relation to the gas bladder of some ophidiiform teleosts osteoblasts that have replaced the osteoclasts. The secondary fibrous protein of collagenous nature (FAURÉ-FREMIET, 1936; found in each scale of L. chalumnae. In L. menadoensis, the (MEUNIER et al., 2015). These dentine plies in the pulp cavity are true osteocytes (Fig. 9E) with a more or less star-shaped in Axelrodichthys is spheritic as in Latimeria’s plates (CUPELLO de Nível Superior – Brasil (CAPES) – Finance Code 001 coelacanths. Scientific Reports, 7: 9244. DOI: al., 1999. Treubia (A Journal on Zoology of the Indo-Australian MILLOT, J., ANTHONY, J. and ROBINEAU, D. 1978. Anatomie de evolutionary approach. Biological Review, 78: 219–249. record of juvenile or small (below 80 cm long) individuals is submersible in a location 360 km away from Manado (FRICKE side of the body was recorded. The individual (ID 2) was and 14 minutes (Fig. 2C; Table 2: E4, ID 3, 4, 5). During this 3). The observation time was the longest of all surveys with Sulawesi Island from the 12th September to the 9th October and R14). Three new individuals (Table 2: ID 26–28) were individuals such as ID 6 on the 12th December 2006 (E5) and behavior. These water currents of different temperatures are chalumnae. Institute of Science for their advice and administrative work to Science, 88: 225–227. we aim to present an overview of the last eighty years is essentially constituted of four axial cartilaginous elements (MILLER and HOBDELL, 1968; GRADY, 1970; HOBDELL and (PARMENTIER et al., 2008). Despite the name, the rocker bone bone does generally not replaced the whole primary bone GARRAULT, 1936). The presence of lepidotrichia with distal basal plate of the scales is also a twisted plywood but its characterizes a plicidentine organization of orthodentine type. outline, and send cytoplasmic extensions in the thickness of et al., 2017). So there is a continuity of the histological (Programa Nacional de Pós Doutorado-PNPD). 10.1038/s41598-017-09327-6. Archipelago), 33: 1–11. Latimeria chalumnae. T. 3. Appareil digestif, téguments, SMITH, J. L. B. 1939. A living fish of the Mesozoic type. virtually absent, the growth, development and breeding et al., 2000). Today 8 individuals were officially caught in the observed for one minute before it hid inside the cave (Table 2: long period of time all individuals stayed near the rock wall four hours and 16 minutes of recording. The temperature (Table 1: R8). On the 24th September 2009, six individuals recognized at different places off Lolak Island (Lolak 1-4). All ID 24 on the 4th May 2012 (E22) swam away. It seemed to caused by the movement of the marine thermocline. During These first observations are potentially crucial since the obtain our research permit. Other thanks go to Mr. OPO, Mr. CUPELLO, C., BRITO, P. M., HERBIN, M., MEUNIER, F. J., (1938–2018) of histological studies of Latimeria’s skeleton. (Fig. 2; MILLOT and ANTHONY, 1958), with pre and post-axial MILLER, 1969; CASTANET et al., 1975; SHELLIS and POOLE, 1978; is not true bony tissue (PARMENTIER et al., 2008), contrary to areas, which can still be recognizable by the presence of actinotrichia in Latimeria, as in the fins of Actinopterygii, is rotation angle seems to be slightly less regular (MEUNIER et al., These primary plies correspond to a simplexodont plicidentine the plate (Fig. 9D, E). Rare lining cells (osteoblasts) are structure of the lung plates in the coelacanths during their EASTMAN, J. T., WITMER, L. M., RIDGELY, R. C. and KUHN, K. HOBDELL, M. H. and MILLER, W. A. 1969. Radiographic écailles. CNRS Edr., Paris. pp. 7–28, 135–139. Nature, 143: 455–456. biology of L. chalumnae remain poorly known. Our knowledge Indonesian seas. However, the details of their habitat have not E2). When a new individual could be identified by the white always keeping their head against the water flow. The water changed up and down several times (Fig. 4). Its difference (Table 2: E11, ID 9, 10, 11, 12, UN 2, 3) were found under an individuals were alone. ID 26 was observed in May and once avoid and escape from the brightness of the light or the sounds our surveys we observed in some area that as the thermocline habitats of the Indonesian coelacanths could be possibly not as REFRY and colleagues at Murex Dive Resort, and DAUD, AL, J ANVIER, P., DUTEL, H. and CLÉMENT, G. 2015.