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The morphology and histology of the scales of Aspidorhynchidae (Actinopterygii, Halecostomi)
THE M O R P H O L O G Y A N D HISTOLOGY OF THE SCALES OF A S P I D O R H Y N C H I D A E (ACTINOPTERYGII, HALECOSTOMI) PAULO M. BRITO & FRhiqOm J. M E U N I E R BRITO P.M. & MEUNIER F.J. 2000. The morphology and histology of the scales of Aspidorhynchidae (Actinopterygii, Halecostomi). [La morphologie et l'histologie des 6cailles d'Aspidorhynchidae (Actinopterygii, Halecostomi)]. GEOBIOS, 33, 1: 105-111. Villeurbanne, le 29.02.2000. Manuscrit ddpos6 le 28.07.1998; accept6 d6finitivement le 09.03.1999. ABSTRACT - The scales of the three genera of aspidorhynchids (Aspidorhynchus, Belonostomus, and Vinctifer) are studied to bring out some characters useful to understand the systematic position of aspidorhinchids within the neopterygians. The scales of the nine species studied are of lepidosteoid type with a ganoine layer overlaying a basal plate made of lamellar bone with canalicules of Williamson. Some species of Aspidorhynchus are devoid of ganoin, whereas others show only a thin ganoine layer. None of the characters found in the scales of aspidorhynchids can be considered as a familial synapomorphy able to place the clade within the teleosts, a situation that does not imply the exclusion of this family from this major group. KEYWORDS: ASPIDORHYNCHIDAE,ASPIDORHYNCHUS, BELONOSTOMUS, VINCTIFER, SCALES,PHYLOGENY. RI~SUMI~ - Les 6cailles des trois genres d'Aspidorhynchidae (Aspidorhynchus, Belonostomus, et Vinctifer) ont 6t6 6tudi6es pour faire ressortir d'6ventuels caract6res permetant de conforter la position syst6matique de cette famille parmi les n6opt6rygiens. Les 6cailles des neuf esp6ces 6tudi6es sont toutes de type ganoide 16pidost6oide, compos6es d'une couche de ganoine recouvrant une plaque basale d'os lamellaire pourvue de canalicules de Williamson. Certaines esp6ces du genre Aspidorhynchus pr6sentent une fine couche de ganoine, d'autres en sont d6pourvues. Aucun des caract6res des 6cailles des Aspidorhynchidae ne peuvent ~tre consid6r6s comme des synapomorphies permettant d'incorporer ce clade aux t616ost6ens, mais cette situation n'implique pas l'exclusion des Aspidorhynchidae de ce groupe majeur des t616ost6ens. MOTS-CLI~S:ASPIDORHYNCHIDAE,ASPIDORHYNCHUS,BELONOSTOMUS,VINCTIFER, I~CAILLES,PHYLOGI~NIE. INTRODUCTION The aspidorhynchids are a diverse group of Halecostomi comprising three distinct genera (Aspidorhynchus, Belonostomus and Vinctifer) with a world-wide distribution and confirmed temporal range from the Middle Jurassic to the Upper Cretaceous (Brito 1988; 1997; Maisey 1991). Aspidorhynchids can be easily recognised by the presence of a long "rostrum" comprising both premaxillaries, a supplementary bone in the lower jaw, the predentary, the presence of deep elongate flank scales, and the posteriorly located dorsal and anal fins (Fig. 1.1). The family Aspidorhynchidae was created by Nicholson & Lydekker (1889) for the genera described by Agassiz (1833-1844) as "Ganoids". Subsequently, aspidorhynchids were treated as a distinct sub-order, the Aethospondyli (Woodward 1895); as holosteans (e.g. Berg 1940); as halecostoms, the term being used, in this case, to include intermediate forms between "holosteans" and the teleosts (Saint-Seine 1949; Arambourg & Bertin 1958; Santos 1985). Now they are considered by the majority of authors as basal teleosts (e.g. Patterson 1973, 1977, 1994; Patterson & Rosen 1977; Maisey 1991; Brito 1992, 1997, in press; De Pinna 1996) although there are still some controversies over this phylogenetic placement (Arratia, in press). Although the extant teleosts form an uncertain
clade, the number of synapomorphies for this group is still unsatisfactory when some Mesozoic taxa, considered by Patterson (1973, 1977) as basal teleosts, are included. Attempting to resolve some of these problems, we undertook a research program with the aim of examining the microstructure of the scales in different neopterygian groups, and especially of the basal teleosts sensu Patterson (op. cit.), trying to elucidate the importance of this anatomical complex in systematic phylogeny. In the present study we attempt to provide a complete description of the scales of the three aspidorhynchid genera (Aspidorhynchus, Belonostomus and Vinctifer) in the hope of understanding their systematic position within the neopterygians. MATERIAL A N D M E T H O D S This study is restricted to the scales of aspidorhynchids. Due to the large number of species and numerous ontogenetic stages available for analysis, we describe the morphological structures as a whole (familial character) followed, when necessary by comments on specific differences. The external surface of ganoin was observed using the scanning electronic microscope (SEM). Ganoin tubercles were measured using the methodology of Gayet & Meunier (1986). Ground cross sections were made using the methodology of Matrajt et al. (1967), modified by Meunier et al. (1978).
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This work is based on specimens belonging to the Universidade do Estado do Rio de Janeiro (UERJ) and the Museum National d'Histoire naturelle, Paris (MNHN); all the scales are sampled on well determined fishes (for a complete list of specimens see Brito 1997). The following taxa were used: Aspidorhynchus acutirostris - Tithonian of Solnhofen, Germany and Upper Kimmeridgian of Cerin, France. Aspidorhynchus cf. euodus - Callovian of Cambridgeshire, England. Aspidorhynchus cf. fisheri - Kimmeridgian of Dorsetshire, England. Aspidorhynchus arawaki - Upper Oxfordian of Pifiar del Rio, Cuba. Belonostomus tenuirostris - Tithonian of Solnhofen, Germany and Upper Kimmeridgian of Cerin, France. Vinctifer comptoni - Albian of Chapada do Araripe, Brazil. Vinctifer longirostris - Aptian of Chapada do Araripe, Brazil. Vinctifer sweeti - Albian of Queensland, Australie. Vinctifer sp.-Albian of Chapada do Araripe, Brazil. RESULTS
EXTERNAL MORPHOLOGY In all aspidorhynchids, the scales are very thick and display a "peg and socket" type of articulation. The flanks of the body are arranged with three rows of hypertrophied scales (Fig. 1.1), all having the same dimension in Aspidorhynchus, or presenting the two superior rows larger than the third, as in Vinctifer and Belonostomus (Brito 1995, 1997; Schultze & Stohr 1996). According to the species or the age of the specimen, the scales are ornamented with tubercles and/or sinuous ridges (Fig. 1.6). Dorsal to the flank scales are three rows of small diamond-like scales that, as well as the top scales, are ornamented with longitudinal parallel ridges separated by narrow intervals. Ventral to the flank scales, there are five or six rows of small, rectangular smooth scales. Articulated odontodes were found only on the surface and posterior margin of caudal scales of Vinctifer comptoni (Fig. 1.2-4), although they are commonly present, covered by the ganoin layer, in all the species of the family (see below). The odontodes are tiny (0,1 to 0,3 mm), hook-like structures always pointing to the rear of the body. These structures surround a pulp cavity and articulate into circular craters in the surface of the scale (Fig. 1.5B). The tubercles on the external surface of the ganoin are characteristic for ganoid elements but they are obvious only in genus Vinctifer. Width and density of the tubercles does not seem to vary significantly within the species of Vinctifer although there are a clear generic differences. The tubercles in V. comptoni are relatively small (4.0 ~m) and their spacing is about 7.0 #m (Fig 1.5A). When present, the tubercles in Belonostomus tenuirostris are not sufficiently well preserved to allow accurate measurments. There are no tubercles on ganoin in
Aspidorhynchids that show a thin layer of ganoin like in juveniles ofAspidorhynchus acutirostris or in A. cf. euodus (see below). HISTOLOGY The general structure of the scales is basicaly similar in the nine species studied. They all show a cellular bony (= osteocytic bone of Weiss & Watabe 1979) basal plate overlain by a more or less thick ganoin layer, generally composed of several sheets between 5 to 16 ttm thick (Fig. 2.1-3). In a juvenile Belonostomus tenuirostris we observed scales with only one birefringent layer 7-10 #m thick.
Aspidorhynchus acutirostris has no ganoin preserved in the scales (Fig. 2.4) (Schultze 1966, 1996), a condition also confirmed in other Aspidorhynchus species such as A. fisheri and A. arawaki; however, a thin ganoin monolayer had been figured by Brito (1997, fig. 36) for a juvenil specimen ofA. acutirostris. In Aspidorhynchus cf. euodus, a very tiny ganoin layer (2-3.5 #m thick) seems to be present in the surface of the stratified basal plate (Fig. 2.5. In fact, there are several "onion-like" layers of ganoin that never overlay completely the older ones. So the ganoin layer appears monostratified. In Vinctifer comptoni the ganoin is also monostratiffed in young specimens (Fig. 2.6). In scales with ganoin ridges, the core of these relief is composed of woven bone which, in this case, appears trapped between the ganoin layer and the subjacent lamellar bone of the basal plate (Fig. 2.1). Independent of the species, when present, the odontodes are fused to the ganoin surface (Fig. 2.7) or occur at depth within the ganoin at its contact with the basal plate (Fig. 2.1). The basal plate of the scales of aspidorhynchids is made of cellular bone. No dentine was observed between the ganoin layer and the basal plate. In the basal plate there are Sharpey's like fibers (Fig. 2.8) that allowed the scales to attach to the dermis and to neighbouring scales. In the nine species examined, the basal plate shows a central area of woven bone with some lamellar bone above (beneath the ganoin layer) and a thicker layer of lamellar bone below. The layers are about 1.6 #m thick (Fig. 2.25). In Vinctifer sweeti and V. comptoni, the basal plate is composed of a lamellar bony tissue (Fig. 2.3,4). The fibril directions of the collagenous layer are orthogonal according to section examined under polarized light: alternating dark and light layers. The mean thickness of these layers is between 1 and 2.6 #m, rarely reaching 3 ttm. In this area, flat lenticular osteocytes are orientated by the organized framework of collagenous fibers. The basal plate is crossed by numerous canalicules of Williamson (Fig. 2.3) and practically lacks any vascular canals; however, when present, they are about 15-17 #m wide. The diameter of the canalicules of Williamson is approximately 1.5-3.5 /tm (1.5-2 #m in Belonostomus tenuirostris). Some of the canalicules of Williamson are ramified; in this case, this structure is a little wider reaching 5-5.5 #m. The canalicules of Williamson are relatively straight in the basal plate, their ramified extremi-
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FIGURE 1 - 1. Vinctifer comptoni. General view of the fish (FMNH-10380a*l) (Bar = 3 cm). 2. Vinctifer comptoni. SEM. A) Odontodes on the surface of the scale; B) detail of an odontode (Bar = 25 ~m). 3. Vinctifer comptoni. SEM. Odontodes on the posterior margin of a scale (Bar = 50 #m). 4. Belonostomus tenuirostris. SEM. Two odontodes (arrows) protrude out of the ganoin layer (Bar = 100 #m). 5. Vinctifer comptoni. SEM. A) Tubercles at the surface of the ganoin layer; B) The same in an area where odontodes have disappeared. Arrows point their base of insertion on the ganoin layer (Bar = 10 ~m). 6. Aspidorhynchus acutirostris. SEM. Ornamentations on the external surface of the scale (Bar = 500 ttm). 1. Vinetifer comptoni. Vue d'ensemble du pqisson (FMNH-10380a*2) (Echelle = 3 cm). 2. Vinctifer comptoni. MEB. A) Odontodes & la surface de l'gcaille; B) dgtail d'un odontode (Echelle = 25 #m). 3. Vinctifer comptoni. MEB. Odontodes sur le bord postgrieur de l~caille (Echelle = 50 ttm). 4. Belonostomus tenuirostris. MEB. Deux odontodes (fl~ches) sortent de la gano~ne (l~chelle = 100 #m). 5. Vinctifer comptoni. MEB. A) Tubercules & la surface de la gano~ne; B) M~me chose dans un secteur oh les odontodes sont tombgs. Les fl~ches pointent la zone d'insertion des odontodes sur la couche de gano~'ne (Echelle = 10 gm). 6. Aspidorhynchus acutirostris. MEB. Ornementations de la surface externe d'une ~caille (Echelle = 500 ttm).
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FIGURE 2 - 1. Vinctifer longirostris (ICH-257.1). Transmitted natural light. The ripples correspond to bony evaginations of the basal plate (bp) overlaid by ganoin (arrow). Two odontodes are shown one inserted at the surface of the ganoin layer (white arrow head), the second just at its contact with the basal plate (black arrow head); see detail in fig. 13 (Bar = 100 ~m). 2. Vinctifer sp. (ICH-258.2). Transmitted polarized (on the left), and natural (on the right) light. Ganoin (g) overlays directly (dentine is lacking) the basal plate (bp) which is constituted of thin bone lamellae (see polarized light) (Bar = 50 #m). 3. Vinctifer sweeti (ICH-262.1) (Lateral line scale). Transmitted polarized (on the left), and natural (on the right) light. The bony walls of the sensory canal (sc) are constituted of secondary bone limited by cementing lines (arrow heads). Numerous canalicules of Williamson (arrows) cross the bony basal plate (bp) (g = ganoine) (Bar = 100 #m). 4. Aspidorhynchus acutirostris (ICH-260.2). Transmitted polarized (on the left), and natural (on the right) light. The ganoin layer is lacking at the surface of the scale (arrow heads). Numerous canalicules of Williamson are seen in the basal plate (Bar = 100 ~m). 5. Aspidorhynchus (?) euodus (ICH-263.3). Transmitted polarized (on the left), and natural (on the right) light. The white and black arrows point to the thin layer of ganoin made of only one strata. The basal plate (bp) shows regular bony lamellae (polarized light) and canalicules of Williamson (arrow heads) (Bar = 75/tin). 6. Vinctifer comptoni, young specimen (ICH-261.1). Transmitted natural light. The ganoin layer (arrow head) has only one strata. The bony basal plate (bp) is crossed by canalicules of Williamson (arrows) (Bar = 100 #m). 7. Vinctifer longirostris (ICH-257.1). Detail of Fig. 7, showing one odontode (empty arrow) inserted in the ganoin layer (g) (bp = basal plate) (Bar -- 25 t~m). 8. Aspidorhynchus (?) euodus (ICH-263.2). Transmitted natural light. Detail of the bony basal plate showing the Sharpey's fibers (arrows) (Bar = 25 ~m). 9. Aspidorhynchus acutirostris (ICH-260.l). Transmitted natural light. Detail of the older part of the basal plate showing isodiametric osteocytes (arrow heads). Arrows point to canalicules of Williamson (Bar = 50 ~m).
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ty extending away from the deep surface of the basal plate, but at a constant distance from the ganoin layer. In fact, they are in a specific zone of the bony basal plate made of woven bone which is isotrope in polarized light. In this zone, osteocytes are isodiametric (Fig. 2.9). In the lateral line scales, the sensory canal is housed in a wide bony canal in which the walls show remodeled bone. The secondary bone is pseudo-lainellar and contrasts strongly with the primary lamellar bone that surround the sensory canal (Fig. 2.3). DISCUSSION
The scales of the aspidorhynchids are of lepidosteoid-type in that the basal lamellar bone layer is directly overlain by ganoin, without an intercalated dentine layer (Goodrich 1907; Schultze 1977, 1996; Sire & Meunier 1994), although Aspidorhynchus acutirostris, A. arawaki and A. fisheri lack the ganoin. The ganoin in the aspidorhynchids has probably an epidermal origin as in extant gars and polypterids (Meunier et al. 1987; Sire et al. 1987; Sire 1994; Zylberberg et al. 1997). As in extant gars, the bony basal plate was deposited first (Nickerson 1893). Effectively the area that houses the terminal ramifications of the canalicules of Williamson corresponds to the initiurn of the scale, the region deposited first during ontogeny. This means that there was a certain time before the deposit of the first bony components of the scales and the first layer of ganoin, since there are several strata oflamellar bone between the initium and the ganoin layer. This process is distinct from that seen in polypterids scales where the first layer to appear during ontogeny is an isopedine layer (Sire 1989, 1990). Another similarity between aspidorhynchids and gars is the presence of odontodes on the surface of the ganoin. Odontodes are known to develop in living gars (Nickerson 1893; Sire 1994) as in Polypterids (Hertwig 1879; G6raudie 1988) although they are often temporary. The presence of these odontodes can be considered as a plesiomorphy. The bony basal plate deposited around this initial nucleation grows more slowly, as indicated by isodiametric osteocytes that become flat, and by the woven collagenous matrix that becomes lamellar (Francillon-Vieillot et al. 1990; Ricql6s et al. 1991). The successive dark and light layers indicate that
the collagenous fibers form an orthogonal "plywood" (Giraud et al. 1978; Meunier & Castanet 1982; Zylberberg et al. 1992). The thickness of each layer is thin (1 to 2,6/tin) whereas in the orthogonal "plywood" of the basal plate in teleostean elasmoid scales it is frequently greater than 3-5 #m and with very thick collagenous fibers (50 to 190 ram). We do not have any information concerning the thickness of collagenous fibers in aspidorhynchids scales but we suppose they were thin, probably less than 50 ram. Thus the bony tissue constituting the basal plate in aspidorhynchids is typically lamellar bone (Francillon-Vieillot et al. 1990; Ricql~s et al. 1991), and not isopedine which is generally constituted of thicker layers (> 3-5 #m) with very thick collagenous fibers (Meunier 1983, 1987; Zylberberg et al. 1992). Moreover, isopedine mineralizes frequently owing to Mandl's corpuscles (Sch~SnbSrner et al. 1981; Meunier 1984; Zylberberg et al. 1992). In the studied material no trace of Mandl's corpuscles has been found. The mineralizing front appears to be very regular, contrary to scales that mineralized with Mandl's corpuscles as, for example, in the scales of the Paleocene Arnia robusta (Meunier & Poplin 1995). The presence of Mandl's corpuscles is a general character of isopedine in elasmoid scales of Actinopterygii (SchSnb6rner et al. 1981; Meunier 1981, 1984; Zylberberg et al. 1992), as well as in Dipnoi (Meunier & Francois 1980) and Latirneria (Meunier 1980; Meunier & Zylberberg 1999) within extant Sarcopterygii and seems to be linked to the diameter of collagenous fibers (Sch6nb~rner et al. 1981; Zylberberg et al. 1992). CONCLUSIONS
None of the characters observed in the scales of aspidorhynchids can be considered autapomorphic for the group; our study have also failed to disclose a single derived character exclusive to aspidorhynchids plus other teleosts. This situation by itself does not imply that aspidorhynchids are not teleosts, but only represents a lack of evidence, regarding this morphological complex, for this systematic placement. Examining the basal teleosts sensu Patterson (1973, 1977) we find that the situation seen in aspidorhynchids is also found in a variety of other taxa considered as basal teleosts. Recently the pachycormids had been excluded from the Teleostei based on phylogenetic analysis (Brito 1997; Arratia in press). Within this clade, Pachy-
FIOURE2 (suite) - 1. Vinctifer longirostris (ICH-257.1). Lumi~re naturelle transmise. Les crates correspondent it des dl~vations osseuses de Ia plaque basale COp) recouvertes par de la gano~ne (fl~che). Deux odontodes sont visibles, Fun insdrd it la surface de la gano~ne (t~te de fl~che blanche), le second au contact de la gano~ne avec la plaque basale (t~te de fl~che noire); voir le dgtail de la fig. 13 (Echelle = 100 #m). 2. Vinctifer sp. (ICH-258.2). Lumi~re polarisde (rnoitid gauche) et lurni~re naturelle transmise (moitid droite). La gano~ne (g) recouvre directement la plaque basale COp)composde de fines lamelles d'os; il n'y a pas de dentine (Echelle = 50 I~m). 3. Vinctifer sweeti (ICH-262.1) (gcaille de la ligne latdrale). Lumi~re polarisde (it gauche) et lurni~re naturelle transrnise (it droite). Les patois osseuses du canal sensoriel (sc) sont constituges d'os secondaire limitd par des lignes cimentantes (t~tes de fl~ches). De nombreux canalieules de Williamson (fl~ches) traversent la plaque basale osseuse COp) (g = gano~ne) (Echelle = 100 ~rn). 4. Aspidorhynchus acutirostris (ICH-260.2). Lurni~re polarisde (maitig gauche) et lumiire naturelle transmise (moitid droite). Il n'y a pas de gano~'ne & la surface de l~caille (t~tes de fl~ches). De nombreux canalicules de Williarnson traversent la plaque basale (E,chelle = 100 p~m). 5. Aspidorhynchus (?) euodus (ICH-263.3). Lurni~re polarisde (moitid gauche) et lurni~re naturelle transrnise (rnoitid droite). Les fl~ches noires et blanches pointent la gano~ne constitude d'une seule strate. La plaque basale COp) prdsente des larnelles osseuses rgguli~res (voir lurni~re polarisde) et des canalicules de Williarnson (t~tes de fl~ches) (Echelle = 75 #m). 6. Vinctifer eomptoni,jeune spdeimen (ICH-261.1). Lumi~re naturelle transmise. La gano~'ne (t~te de fl~che) est constitude d'une seule strafe. La plaque basale osseuse COp)est traversge par des canalicules de Williarnson (fl~ches) (Echelle = 100 ~m). 7. Vinctifer longirostris (ICH-257.1). Dgtail de la Fig. 7, montrant un odontode (fl~che creuse) insgrd darts la couche de gano~ne (g) Cop = plaque basale) (Echelle = 25 ~rn). 8. Aspidorhynchus (?) euodus ([CH-263.2). Lumi~re naturelle transmise. D~tail de la plaque basale osseuse montrant des fibres de Sharpey (fl~ches) (Echelle = 25 #m). 9. Aspidorhynchus acutirostris (ICH-260.1). Lurni~re naturelle transmise. Ddtail montrant des ostdocytes isodiamdtriques (t~tes de fl~ches) et des canalicules de Williamson darts la zone la plus ancienne de la plaque basale (Echelle = 50 p.m).
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cormus curtus, Saurostornus esocinus, Hypsocormus insignis and Euthynotus incognitus show radial structures that indicate a tendency to evolve into amioid-like scales (Schultze 1966, 1996).
Pholidophorus bechei has ganoid, lepidosteoid-type scales, a pattern confirmed in another Pholidophorus from the Upper Liassic of Normandy (Meunier & Brito in prep.). Pholidophorus bechei is corroborated as a basal taxon teleost although the whole family Pholidophoridae as well as other "pholidophoriforms" require revision (Arratia in press). A major problem in demonstrating the monophyly of the Teleostei when Mesozoic clades are included, lies in the difficulty of ascertaining the exact level of generality of the teleostean synapomorphies and in determining which are the "valid" synapomorphies. Recently, Brito (1997, in press) reviewed the aspidorhynchids and suggested, despite the many conflicting characters, retaining aspidorhynchids as basal teleosts based on, at least, one character: the presence of paired uroneurals in Vinctifer and Aspidorhynchus. Accepting this optic, we can conclude from the aspidorhynchids scales that: - Aspidorhynchids present typical ganoid, lepidosteoid scales. Aspidorhynchus species having lost the ganoin secondarily; - The odontodes found on the ganoin surface in aspidorhynchids are here interpreted as a plesiomorphic character find in "ganoid" fishes; these structures being homologous to the odontodes of the scales of extant polypterids and gars; - The bony basal plate composed of lamellar bone can give rise directly to the isopedine of elasmoid scales with augmentation a) of thickness of strata and b) probably of fibres diameter, this last one being linked with the presence of Mandl's corpuscles which are responsible of the progression of mineralization; - Structures like the canalicules of Williamson were considered as typical "holostean" features (gars plus Mesozoic taxa), however they are also find at the pholidophorid level what suggest a plesiomorphic feature within the actinopterygians; - Finally, accepting the aspidorhynchids as basal teleosts, we must hypothesise the orthogonal "plywood" as the plesiomorphic state, the presence of a helicoidal "plywood" being the synapomorphic state for more advanced teleosts; accepting this hypothesis, we must interpret the orthogonal "plywood" of perciformes (Meunier & Castanet 1982) as a feversal character. Another question arises: is the orthogonal "plywood" of aspidorhynchids homologous to the isospedine of polypterids' scales as suggested by Sire (1989, 1990), or to both isopedine and bony basal plate or to bony basal plate only? Effectively, isopedine formation is still unknown in the ganoid scales of taxa that are placed between the polypterid branch and the basal teleosts in the phylogenetical tree of Actinopterygii (Lauder & Liem 1983; Patterson 1994; Brito 1997). A c k n o w l e d g e m e n t s - We thanks C. Weber and M. Lemoine for technical assistance, and Mrs. V.G. da Silva and D. Martill for comenting various drafts of this work. P.M.B. examined different collections of aspidorhynchids over the last seven years
and acknowledge t h e help of m a n y curators, specially Prof. R. Billard and Dr. S. Wenz (Paris), Prof. G. A r r a t i a (Berlin), Dr. J. Tyler (Washington, D.C.), and Dr. G. Viohl (Eichstfitt). Mr. Steve Etches and Dr. D. Martill provided s a m p l e s from the Callovian and K i m m e r i d g i a n of England. P.M. B, is finantially supported by the CNPq, Brazilian Federal Government.
REFERENCES AGASSIZL. 1833-1844 - Recherches sur les Poissons fossiles. 5 vols., 1420 p., avec suppl6ment, Neuch~tel. ARAMBOURG C. & BERTIN L. 1958 - Super-Ordre des Holost6ens et des Hal6costomes (Holostei et Halecostomi). In GRASSE P.P. (ed.), Traitd de Zoologie, 13, 3: 2173-2203. Masson & Cie, Paris. AR~TL~ G. (in press) - The monophyly of teleostei and stem group teleosts. Consensus and disagreements. In ARRATIA G. & SCHULTZE H.P. (eds), Mesozoic fishes - Systematics and The Fossil Record, M6nchen (Verlag Dr. F. Pfeil). BEaG L.S. 1940 - Classification of fishes, both recent and fossils. Trudy zoologicestogo Instituta Leningrad, 5: 87-517. BRITO P.M. 1988 - La structure du suspensorium de Vinctifer, poisson actinopt6rygien m6sozoique: remarques sur les implications phylog6n6tiques. Geobios, 21: 819-823. ..... 1992 - L'endocr~ne et le moulage endocr~nien de Vinctifer comptoni (Actinopterygii-Aspidorhynchiformes) du Cr6tac6 inf~rieur du Br6sil. Annales de Paldontologie (VertdbrdsInvertdbrds), 78: 129-157. ..... 1995 - R6vision des Aspidorhynchidae (Pisces, Actinopterygii) du M6sozoYque: ost6ologie et relations phylog6n6tiques. Th6se de Doctorat, Mus6um national d'Histoire naturelle, Paris. 188 p., (in6dit). ..... 1997 - R6vision des Aspidorhynchidae (Pisces, Actinopterygii) du M6sozoique: ost6ologie, relations phylog6n6tiques, donn6es environnementales et biog6ographiques. Geodiversitas, 19: 681-772. ..... (in press) - The caudal skeleton of aspidorhynchids (Actinopterygii: Halecostomi): phylogenetic implications. In ARRATIAG. & SCHULTZEH.P. (eds), Mesozoic fishes - Systematics and The Fossil Record, Verlag Dr. F. Pfeil, Mtinchen. DE PINNAM.C.C. 1996 - Teleostean Monophyly. In M.L.J. STIASSNY, L.R. PARENTI & G.D. JOHNSOn (eds), Interrelationships of Fishes: 147-162. FRANCILLON-VIEILLOT H., BUFFRI~NIL V. DE, CASTANET J., GERAUDIE J., MEUNIER F.J., SIRE J.Y., ZYLBERBERGL. & RICQLESA. de 1990 Microstructure and mineralization of Vertebrate skeletal tissues. In J.G. CARTER(ed.), Skeletal biomineralization: patterns, processes and evolutionary trends, 1: 471-530, Van Nostrand Reinhold, New-York. CAWT M. & MEUNIER F.J. 1986 - Apport de l'6tude de l'ornemenration microscopique de la ganoine dans la d6termination de l'apparence g6n6rique et/ou sp6cifique des 6cailles isol6es. Comptes Rendus de l'Acaddmie des Sciences de Paris, 2, 363: 1259-1261. GEr~UDIE J. 1988. - Fine structural peculiarities of the pectoral fin dermoskeleton of two Brachiopterygii, Polypterus senegalus and Calamoichthys calabaricus (Pisces, osteichthyes). Anatomical Record, 221: 455-468. GIRAUD M.M., CASTANET J., MEUNIER F.J. & BOULIGAND Y. 1978 - The fibrous structure of coelacanth scales: a twisted "plywood". Tissue and Cell, 10: 671-686. GOODRICH E.S. 1907 - On the scales offish, living and extinct, and their importance in classification. Proceedings of the Zoological Society of London, 2: 751-774. HERTWIG O. 1879. - Ueber das Hautskelett der Fische. Morphologisches Jahrbuch, 5, 21 p. LAUDER G.V. & LIEM K.F. 1983 - The evolution and interrelationships of the actinopterygian fishes. Bulletin of the Museum of Comparative Zoology, 150: 95-197. MAISEYJ. G. 1991 - Vinctifer. In J.G. MAISEY(ed.), Santana Fossils, 170-189, New York, TFP. MATRAJT H., BORDIER P., MARTIN J. & HIOCO D. 1967 - Technique pour l'inclusion de biopsies osseuses non d6calcifi6es. Journal de Microscopie, 6: 499-504. MEUNIER F.J. 1980 - Les relations isop6dine-tissu osseux dans le post-temporal et les 6cailles de la ligne lat6rale de Latimeria ehalumnae (SMITH).Zoologica Scripta, 9: 307-317. ..... 1983 - Les tissus osseux des ost6ichthyens. Structure, gen6se, croissance et 6volution. Archives et Documents,
111
Micro-Edition, Institut Ethnologique, Musgum national d'Histoire naturelIe, SN, 82-600-328. ..... 1984 - Spatial organization a n d m i n e r a l i z a t i o n of t h e b a s a l plate of elasmoid scales in osteichthyans. American Zoologist, 24: 953-964. ..... 1987.- Os cellulaire, os acellulaire et t i s s u s d@rivds chez les ost~ichthyens: les p h ~ n o m ~ n e s de l'acellularisation et de la perte de min~ralisation. L'Annde Biologique, 26: 201-233. ..... & CASTANETJ. 1982 - O r g a n i s a t i o n spatiale des fibres de collag~ne de la plaque b a s a l e des 6cailles des %l@ost~ens. Zoologica Scripta, 11: 141-153. ..... & FRANCois Y. 1980 - U o r g a n i s a t i o n spatiale des fibres collag~nes et la min~ralisation des ~cailles des d i p n e u s t e s actuels. Bulletin de la Socidtd zoologique de France, 105: 215226. ..... , FRANQOISY. & CASTANETJ. 1978- ]~tude histologique et microradiographique des @cailles de quelques actinopt@rygiens primitifs actuels. Bulletin de la Socidtd zoologique de France, 103: 309-318. ..... , GAYET M., G~RAUDIE J., SIRX J.Y. & ZYLBEasERa L. 1987 Donn~es u l t r a s t r u c t u r a l e s s u r la ganoYne du d e r m o s q u e l e t t e des actinopt@rygiens primitifs. In RUSSELL D.E., SANTOROJ.-P. & SIGOGNEAu-RusSELLD. (eds), Teeth revisited, Proceedings of t h e VIIth Inter. Syrup. on D e n t a l Morphology, Paris 1986. Mgmoires du Musdum national d'Histoire natureIle, C 53: 7783. & POPLIN C. 1995 - Paleohistological s t u d y of t h e scales of Amia robusta PRIEM, 1901, Amiidae from t h e T h a n e t i a n (Paleocene) of C e r n a y (France). Geobios, M@m. sp. 19: 39-43. ..... & ZYLBER~ERGL. 1999 - The s t r u c t u r e of t h e external layer a n d of t h e odontodes of scales in Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) revisited u s i n g scann i n g a n d t r a n s m i s s i o n electron microscopy. In SERET B. & SIRE J.-Y. (eds), Proceedings of the 5th Indo-Pacific Fish Conference, Noumga, 1997, Soci~t@ FranCaise d'Ichtyologie, Paris. NICHOLSON H.A. & LYDEKKERR. 1889 - A manual ofpalaeontology. 2nd. ed., 1624 p. E d i n b u r g h a n d London. NICK~RSON W.S. 1893 - T h e d e v e l o p m e n t of t h e scales of Lepidosteus. Bulletin of the Museum of Comparative Zoology, 24: 115-139. PATTERSON C. 1973 - I n t e r r e l a t i o n s h i p s of holosteans. In GREENWOODP.M., WILES R.S. & C. PATTERSON(eds), Interelationships of fishes: 233-305. Academic Press, London. ..... 1977 - The contribution of paleontology to Teleostean phylogeny. In M.K. HECHT, P.C. GOODY & B.M. HECHT (eds), Major patterns in Vertebrate evolution: 579-643, New York. ..... 1994 - Bony fishes. In D.R. PROTHERO & R.M. SCHOCH (eds), .
.
.
.
.
Major patterns in Vertebrate evolution, Short Courses Paleontology, 7: 57-84. Paleontological Society, Tennessee. & ROSEN D. 1977 - Review of Ichthyodectiform a n d other Mesozoic teleost fishes a n d t h e theory a n d practice of classifying fossils. Bulletin of the American Museum of Natural History, 158 : 81-172. RICQLES A. DE, MEUNmR F.J., CASTANETJ. & FRANClLLON-VIEILLOTH. 1991 - Comparative m i c r o s t r u c t u r e of bone. In B.K. HALL (ed.), Bone, 3, 77 p. CRC Press, Boca Raton. SAINT-SEINE P. 1949 - Les poissons des calcaires lltographiques de Cerin (Ain). Nouvelles Archives du Musdum d'Histoire naturelle de Lyon, 2, 357 p. SANTOS R. SILVA DA 1985 - Nova caracterizagao do g6nero Vinctifer JORDAN, 1919. In ColetSnia de trabalhos paleontologicos, D e p a r t a m e n t o NacionaI de Produ~ao Mineral: 151-154, Brasilia. SCHONB(~RNERA.A., MEUNIER F.J. & CASTANETg. 1981 - The fine s t r u c t u r e of calcified Mandl's corpuscles in teleosts fish scales. Tissue and Cell, 13: 589-597. .
.
.
.
.
SCHULWZE H.-P. 1966 - M o r p h o l o g i s c h e u n d h i s t o l o g i s c h e U n t e r s u c h u n g e n a n S c h u p p e n mesozoischer actinopterygier (Obergang yon Ganoid- zu R u n d s c h u p p e n ) . Neues Jahrbuch fiir Geologie und Paliiontologie, 126: 232-314. ..... 1977 - A u s g a n s f o r m u n d E n t w i c k l u n g der r h o m b i s c h e n S c h u p p e n der Osteichthyes (Pisces). Paliiontologische Zeitschrift, 51: 152-168. ..... 1996 - The scales of Mesozoic actinopterygians. In ARRATI*G. & G. VIOL (eds), Mesozoic fishes - Systematics and Paleoecology: 83-93. Verlag Dr. F. Pfeil, M u n c h e n . ..... & STOHR D. 1996 - Vinctifer (Pisces, Aspidorhynchidae) a u s der U n t e r k r e i d e (oberes Aptium) yon Kolumbien. Neues Jahrbuch f~r Geologie und Pal(tontologie, 199: 395-415. SIRE J.Y. 1989 - Scales in y o u n g Polypterus senegaIus are elasmold: new phylogenetic implications. American Journal of Anatomy, 186: 315-323. ..... 1990 - From ganoid to elasmoid scales in t h e actinopterygian fishes. Netherland Journal of Zoology, 40: 75-92. ..... 1994 - Light and T E M s t u d y of n o n r e g e n e r a t e d a n d experim e n t a l l y r e g e n e r a t e d scales ofLepisosteus oculatus (Holostei) with particular attention to ganoYne formation. Anatomical Record, 240: 189-207. ..... , GI~RAUDIEJ., MEUNIER F.J. & ZYLBERBERGL. 1987 - On the origin of ganoine: histological a n d u l t r a s t r u c t u r a l d a t a on t h e e x p e r i m e n t a l regeneration of t h e scales of Calamoichthys ealabaricus (Osteichthyes, Brachyopterygii, Polypteridae). American Journal of Anatomy, 180: 391-402. • MEUNIER F.J. 1994 - The canaliculi of Williamson in holost e a n bone (Osteichthyes, Actinopterygii): a s t r u c t u r a l a n d u l t r a s t r u c t u r a l study. Acta Zoologica, 75: 235-247. WEiss R.E. & WATABEN. 1979 - Studies on t h e biology o f f i s h bone. III- U l t r a s t r u c t u r e of osteogenesis a n d resorption in osteocytic (cellular) a n d anosteocytic (acellular) bones. Calcified Tissue International, 28: 43-56. WOODWARDSA.S. 1895 - Catalogue of fossil fishes in the British Museum, Pt. 3. xiii + 544 p, London. ZYLBERBERGL., GERAUDIEJ., MEUNIER F.J. & SIRE J.Y. 1992 - Biomineralization in t h e i n t e g u m e n t a l skeleton of the living lower Vertebrates. In I4~LL B.K. (ed.), Bone, 4: 171-224, CRC Press. ..... , SIRE J.Y. & N~'~cI A. 1997 - Detection of amelogenin-like proteins in t h e ganoine of experimentally r e g e n e r a t i n g scales of Calamoichthys calabaricus, a primitive actinopterygian fish. Anatomical Record, 249: 86-95. .
.
.
.
.
P.M. B R I T O D e p a r t a m e n t o de Biologia A n i m a l e Vegetal U n i v e r s i d a d e do E s t a d o do Rio de J a n e i r o r u a Sao F r a n c i s c o Xavier 524 Rio de J a n e i r o , Brazil et L a b o r a t o i r e d'Ichtyologie g~ndrale et appliqu4e M u s 6 u m n a t i o n a l d'Histoire n a t u r e l l e 43 r u e C u v i e r F-75231 P a r i s cedex 05 F.J. M E U N I E R C N R S 1451, L a b o r a t o i r e d'Ichtyologie g@n~rale et appliqu@e M u s 6 u m n a t i o n a l d'Histoire n a t u r e l l e 43 r u e C u v i e r F-75231 P a r i s cedex 05 et U M A C N R S 8560, L a b o r a t o i r e d ' A n a t o m i e compar~e U n i v e r s i t ~ D. D i d e r o t 2 place J u s s i e u F-75251 P a r i s cedex 05
clade, the number of synapomorphies for this group is still unsatisfactory when some Mesozoic taxa, considered by Patterson (1973, 1977) as basal teleosts, are included. Attempting to resolve some of these problems, we undertook a research program with the aim of examining the microstructure of the scales in different neopterygian groups, and especially of the basal teleosts sensu Patterson (op. cit.), trying to elucidate the importance of this anatomical complex in systematic phylogeny. In the present study we attempt to provide a complete description of the scales of the three aspidorhynchid genera (Aspidorhynchus, Belonostomus and Vinctifer) in the hope of understanding their systematic position within the neopterygians. MATERIAL A N D M E T H O D S This study is restricted to the scales of aspidorhynchids. Due to the large number of species and numerous ontogenetic stages available for analysis, we describe the morphological structures as a whole (familial character) followed, when necessary by comments on specific differences. The external surface of ganoin was observed using the scanning electronic microscope (SEM). Ganoin tubercles were measured using the methodology of Gayet & Meunier (1986). Ground cross sections were made using the methodology of Matrajt et al. (1967), modified by Meunier et al. (1978).
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This work is based on specimens belonging to the Universidade do Estado do Rio de Janeiro (UERJ) and the Museum National d'Histoire naturelle, Paris (MNHN); all the scales are sampled on well determined fishes (for a complete list of specimens see Brito 1997). The following taxa were used: Aspidorhynchus acutirostris - Tithonian of Solnhofen, Germany and Upper Kimmeridgian of Cerin, France. Aspidorhynchus cf. euodus - Callovian of Cambridgeshire, England. Aspidorhynchus cf. fisheri - Kimmeridgian of Dorsetshire, England. Aspidorhynchus arawaki - Upper Oxfordian of Pifiar del Rio, Cuba. Belonostomus tenuirostris - Tithonian of Solnhofen, Germany and Upper Kimmeridgian of Cerin, France. Vinctifer comptoni - Albian of Chapada do Araripe, Brazil. Vinctifer longirostris - Aptian of Chapada do Araripe, Brazil. Vinctifer sweeti - Albian of Queensland, Australie. Vinctifer sp.-Albian of Chapada do Araripe, Brazil. RESULTS
EXTERNAL MORPHOLOGY In all aspidorhynchids, the scales are very thick and display a "peg and socket" type of articulation. The flanks of the body are arranged with three rows of hypertrophied scales (Fig. 1.1), all having the same dimension in Aspidorhynchus, or presenting the two superior rows larger than the third, as in Vinctifer and Belonostomus (Brito 1995, 1997; Schultze & Stohr 1996). According to the species or the age of the specimen, the scales are ornamented with tubercles and/or sinuous ridges (Fig. 1.6). Dorsal to the flank scales are three rows of small diamond-like scales that, as well as the top scales, are ornamented with longitudinal parallel ridges separated by narrow intervals. Ventral to the flank scales, there are five or six rows of small, rectangular smooth scales. Articulated odontodes were found only on the surface and posterior margin of caudal scales of Vinctifer comptoni (Fig. 1.2-4), although they are commonly present, covered by the ganoin layer, in all the species of the family (see below). The odontodes are tiny (0,1 to 0,3 mm), hook-like structures always pointing to the rear of the body. These structures surround a pulp cavity and articulate into circular craters in the surface of the scale (Fig. 1.5B). The tubercles on the external surface of the ganoin are characteristic for ganoid elements but they are obvious only in genus Vinctifer. Width and density of the tubercles does not seem to vary significantly within the species of Vinctifer although there are a clear generic differences. The tubercles in V. comptoni are relatively small (4.0 ~m) and their spacing is about 7.0 #m (Fig 1.5A). When present, the tubercles in Belonostomus tenuirostris are not sufficiently well preserved to allow accurate measurments. There are no tubercles on ganoin in
Aspidorhynchids that show a thin layer of ganoin like in juveniles ofAspidorhynchus acutirostris or in A. cf. euodus (see below). HISTOLOGY The general structure of the scales is basicaly similar in the nine species studied. They all show a cellular bony (= osteocytic bone of Weiss & Watabe 1979) basal plate overlain by a more or less thick ganoin layer, generally composed of several sheets between 5 to 16 ttm thick (Fig. 2.1-3). In a juvenile Belonostomus tenuirostris we observed scales with only one birefringent layer 7-10 #m thick.
Aspidorhynchus acutirostris has no ganoin preserved in the scales (Fig. 2.4) (Schultze 1966, 1996), a condition also confirmed in other Aspidorhynchus species such as A. fisheri and A. arawaki; however, a thin ganoin monolayer had been figured by Brito (1997, fig. 36) for a juvenil specimen ofA. acutirostris. In Aspidorhynchus cf. euodus, a very tiny ganoin layer (2-3.5 #m thick) seems to be present in the surface of the stratified basal plate (Fig. 2.5. In fact, there are several "onion-like" layers of ganoin that never overlay completely the older ones. So the ganoin layer appears monostratified. In Vinctifer comptoni the ganoin is also monostratiffed in young specimens (Fig. 2.6). In scales with ganoin ridges, the core of these relief is composed of woven bone which, in this case, appears trapped between the ganoin layer and the subjacent lamellar bone of the basal plate (Fig. 2.1). Independent of the species, when present, the odontodes are fused to the ganoin surface (Fig. 2.7) or occur at depth within the ganoin at its contact with the basal plate (Fig. 2.1). The basal plate of the scales of aspidorhynchids is made of cellular bone. No dentine was observed between the ganoin layer and the basal plate. In the basal plate there are Sharpey's like fibers (Fig. 2.8) that allowed the scales to attach to the dermis and to neighbouring scales. In the nine species examined, the basal plate shows a central area of woven bone with some lamellar bone above (beneath the ganoin layer) and a thicker layer of lamellar bone below. The layers are about 1.6 #m thick (Fig. 2.25). In Vinctifer sweeti and V. comptoni, the basal plate is composed of a lamellar bony tissue (Fig. 2.3,4). The fibril directions of the collagenous layer are orthogonal according to section examined under polarized light: alternating dark and light layers. The mean thickness of these layers is between 1 and 2.6 #m, rarely reaching 3 ttm. In this area, flat lenticular osteocytes are orientated by the organized framework of collagenous fibers. The basal plate is crossed by numerous canalicules of Williamson (Fig. 2.3) and practically lacks any vascular canals; however, when present, they are about 15-17 #m wide. The diameter of the canalicules of Williamson is approximately 1.5-3.5 /tm (1.5-2 #m in Belonostomus tenuirostris). Some of the canalicules of Williamson are ramified; in this case, this structure is a little wider reaching 5-5.5 #m. The canalicules of Williamson are relatively straight in the basal plate, their ramified extremi-
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FIGURE 1 - 1. Vinctifer comptoni. General view of the fish (FMNH-10380a*l) (Bar = 3 cm). 2. Vinctifer comptoni. SEM. A) Odontodes on the surface of the scale; B) detail of an odontode (Bar = 25 ~m). 3. Vinctifer comptoni. SEM. Odontodes on the posterior margin of a scale (Bar = 50 #m). 4. Belonostomus tenuirostris. SEM. Two odontodes (arrows) protrude out of the ganoin layer (Bar = 100 #m). 5. Vinctifer comptoni. SEM. A) Tubercles at the surface of the ganoin layer; B) The same in an area where odontodes have disappeared. Arrows point their base of insertion on the ganoin layer (Bar = 10 ~m). 6. Aspidorhynchus acutirostris. SEM. Ornamentations on the external surface of the scale (Bar = 500 ttm). 1. Vinetifer comptoni. Vue d'ensemble du pqisson (FMNH-10380a*2) (Echelle = 3 cm). 2. Vinctifer comptoni. MEB. A) Odontodes & la surface de l'gcaille; B) dgtail d'un odontode (Echelle = 25 #m). 3. Vinctifer comptoni. MEB. Odontodes sur le bord postgrieur de l~caille (Echelle = 50 ttm). 4. Belonostomus tenuirostris. MEB. Deux odontodes (fl~ches) sortent de la gano~ne (l~chelle = 100 #m). 5. Vinctifer comptoni. MEB. A) Tubercules & la surface de la gano~ne; B) M~me chose dans un secteur oh les odontodes sont tombgs. Les fl~ches pointent la zone d'insertion des odontodes sur la couche de gano~'ne (Echelle = 10 gm). 6. Aspidorhynchus acutirostris. MEB. Ornementations de la surface externe d'une ~caille (Echelle = 500 ttm).
108
.... ~ ; ~
|
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2,
FIGURE 2 - 1. Vinctifer longirostris (ICH-257.1). Transmitted natural light. The ripples correspond to bony evaginations of the basal plate (bp) overlaid by ganoin (arrow). Two odontodes are shown one inserted at the surface of the ganoin layer (white arrow head), the second just at its contact with the basal plate (black arrow head); see detail in fig. 13 (Bar = 100 ~m). 2. Vinctifer sp. (ICH-258.2). Transmitted polarized (on the left), and natural (on the right) light. Ganoin (g) overlays directly (dentine is lacking) the basal plate (bp) which is constituted of thin bone lamellae (see polarized light) (Bar = 50 #m). 3. Vinctifer sweeti (ICH-262.1) (Lateral line scale). Transmitted polarized (on the left), and natural (on the right) light. The bony walls of the sensory canal (sc) are constituted of secondary bone limited by cementing lines (arrow heads). Numerous canalicules of Williamson (arrows) cross the bony basal plate (bp) (g = ganoine) (Bar = 100 #m). 4. Aspidorhynchus acutirostris (ICH-260.2). Transmitted polarized (on the left), and natural (on the right) light. The ganoin layer is lacking at the surface of the scale (arrow heads). Numerous canalicules of Williamson are seen in the basal plate (Bar = 100 ~m). 5. Aspidorhynchus (?) euodus (ICH-263.3). Transmitted polarized (on the left), and natural (on the right) light. The white and black arrows point to the thin layer of ganoin made of only one strata. The basal plate (bp) shows regular bony lamellae (polarized light) and canalicules of Williamson (arrow heads) (Bar = 75/tin). 6. Vinctifer comptoni, young specimen (ICH-261.1). Transmitted natural light. The ganoin layer (arrow head) has only one strata. The bony basal plate (bp) is crossed by canalicules of Williamson (arrows) (Bar = 100 #m). 7. Vinctifer longirostris (ICH-257.1). Detail of Fig. 7, showing one odontode (empty arrow) inserted in the ganoin layer (g) (bp = basal plate) (Bar -- 25 t~m). 8. Aspidorhynchus (?) euodus (ICH-263.2). Transmitted natural light. Detail of the bony basal plate showing the Sharpey's fibers (arrows) (Bar = 25 ~m). 9. Aspidorhynchus acutirostris (ICH-260.l). Transmitted natural light. Detail of the older part of the basal plate showing isodiametric osteocytes (arrow heads). Arrows point to canalicules of Williamson (Bar = 50 ~m).
109
ty extending away from the deep surface of the basal plate, but at a constant distance from the ganoin layer. In fact, they are in a specific zone of the bony basal plate made of woven bone which is isotrope in polarized light. In this zone, osteocytes are isodiametric (Fig. 2.9). In the lateral line scales, the sensory canal is housed in a wide bony canal in which the walls show remodeled bone. The secondary bone is pseudo-lainellar and contrasts strongly with the primary lamellar bone that surround the sensory canal (Fig. 2.3). DISCUSSION
The scales of the aspidorhynchids are of lepidosteoid-type in that the basal lamellar bone layer is directly overlain by ganoin, without an intercalated dentine layer (Goodrich 1907; Schultze 1977, 1996; Sire & Meunier 1994), although Aspidorhynchus acutirostris, A. arawaki and A. fisheri lack the ganoin. The ganoin in the aspidorhynchids has probably an epidermal origin as in extant gars and polypterids (Meunier et al. 1987; Sire et al. 1987; Sire 1994; Zylberberg et al. 1997). As in extant gars, the bony basal plate was deposited first (Nickerson 1893). Effectively the area that houses the terminal ramifications of the canalicules of Williamson corresponds to the initiurn of the scale, the region deposited first during ontogeny. This means that there was a certain time before the deposit of the first bony components of the scales and the first layer of ganoin, since there are several strata oflamellar bone between the initium and the ganoin layer. This process is distinct from that seen in polypterids scales where the first layer to appear during ontogeny is an isopedine layer (Sire 1989, 1990). Another similarity between aspidorhynchids and gars is the presence of odontodes on the surface of the ganoin. Odontodes are known to develop in living gars (Nickerson 1893; Sire 1994) as in Polypterids (Hertwig 1879; G6raudie 1988) although they are often temporary. The presence of these odontodes can be considered as a plesiomorphy. The bony basal plate deposited around this initial nucleation grows more slowly, as indicated by isodiametric osteocytes that become flat, and by the woven collagenous matrix that becomes lamellar (Francillon-Vieillot et al. 1990; Ricql6s et al. 1991). The successive dark and light layers indicate that
the collagenous fibers form an orthogonal "plywood" (Giraud et al. 1978; Meunier & Castanet 1982; Zylberberg et al. 1992). The thickness of each layer is thin (1 to 2,6/tin) whereas in the orthogonal "plywood" of the basal plate in teleostean elasmoid scales it is frequently greater than 3-5 #m and with very thick collagenous fibers (50 to 190 ram). We do not have any information concerning the thickness of collagenous fibers in aspidorhynchids scales but we suppose they were thin, probably less than 50 ram. Thus the bony tissue constituting the basal plate in aspidorhynchids is typically lamellar bone (Francillon-Vieillot et al. 1990; Ricql~s et al. 1991), and not isopedine which is generally constituted of thicker layers (> 3-5 #m) with very thick collagenous fibers (Meunier 1983, 1987; Zylberberg et al. 1992). Moreover, isopedine mineralizes frequently owing to Mandl's corpuscles (Sch~SnbSrner et al. 1981; Meunier 1984; Zylberberg et al. 1992). In the studied material no trace of Mandl's corpuscles has been found. The mineralizing front appears to be very regular, contrary to scales that mineralized with Mandl's corpuscles as, for example, in the scales of the Paleocene Arnia robusta (Meunier & Poplin 1995). The presence of Mandl's corpuscles is a general character of isopedine in elasmoid scales of Actinopterygii (SchSnb6rner et al. 1981; Meunier 1981, 1984; Zylberberg et al. 1992), as well as in Dipnoi (Meunier & Francois 1980) and Latirneria (Meunier 1980; Meunier & Zylberberg 1999) within extant Sarcopterygii and seems to be linked to the diameter of collagenous fibers (Sch6nb~rner et al. 1981; Zylberberg et al. 1992). CONCLUSIONS
None of the characters observed in the scales of aspidorhynchids can be considered autapomorphic for the group; our study have also failed to disclose a single derived character exclusive to aspidorhynchids plus other teleosts. This situation by itself does not imply that aspidorhynchids are not teleosts, but only represents a lack of evidence, regarding this morphological complex, for this systematic placement. Examining the basal teleosts sensu Patterson (1973, 1977) we find that the situation seen in aspidorhynchids is also found in a variety of other taxa considered as basal teleosts. Recently the pachycormids had been excluded from the Teleostei based on phylogenetic analysis (Brito 1997; Arratia in press). Within this clade, Pachy-
FIOURE2 (suite) - 1. Vinctifer longirostris (ICH-257.1). Lumi~re naturelle transmise. Les crates correspondent it des dl~vations osseuses de Ia plaque basale COp) recouvertes par de la gano~ne (fl~che). Deux odontodes sont visibles, Fun insdrd it la surface de la gano~ne (t~te de fl~che blanche), le second au contact de la gano~ne avec la plaque basale (t~te de fl~che noire); voir le dgtail de la fig. 13 (Echelle = 100 #m). 2. Vinctifer sp. (ICH-258.2). Lumi~re polarisde (rnoitid gauche) et lurni~re naturelle transmise (moitid droite). La gano~ne (g) recouvre directement la plaque basale COp)composde de fines lamelles d'os; il n'y a pas de dentine (Echelle = 50 I~m). 3. Vinctifer sweeti (ICH-262.1) (gcaille de la ligne latdrale). Lumi~re polarisde (it gauche) et lurni~re naturelle transrnise (it droite). Les patois osseuses du canal sensoriel (sc) sont constituges d'os secondaire limitd par des lignes cimentantes (t~tes de fl~ches). De nombreux canalieules de Williamson (fl~ches) traversent la plaque basale osseuse COp) (g = gano~ne) (Echelle = 100 ~rn). 4. Aspidorhynchus acutirostris (ICH-260.2). Lurni~re polarisde (maitig gauche) et lumiire naturelle transmise (moitid droite). Il n'y a pas de gano~'ne & la surface de l~caille (t~tes de fl~ches). De nombreux canalicules de Williarnson traversent la plaque basale (E,chelle = 100 p~m). 5. Aspidorhynchus (?) euodus (ICH-263.3). Lurni~re polarisde (moitid gauche) et lurni~re naturelle transrnise (rnoitid droite). Les fl~ches noires et blanches pointent la gano~ne constitude d'une seule strate. La plaque basale COp) prdsente des larnelles osseuses rgguli~res (voir lurni~re polarisde) et des canalicules de Williarnson (t~tes de fl~ches) (Echelle = 75 #m). 6. Vinctifer eomptoni,jeune spdeimen (ICH-261.1). Lumi~re naturelle transmise. La gano~'ne (t~te de fl~che) est constitude d'une seule strafe. La plaque basale osseuse COp)est traversge par des canalicules de Williarnson (fl~ches) (Echelle = 100 ~m). 7. Vinctifer longirostris (ICH-257.1). Dgtail de la Fig. 7, montrant un odontode (fl~che creuse) insgrd darts la couche de gano~ne (g) Cop = plaque basale) (Echelle = 25 ~rn). 8. Aspidorhynchus (?) euodus ([CH-263.2). Lumi~re naturelle transmise. D~tail de la plaque basale osseuse montrant des fibres de Sharpey (fl~ches) (Echelle = 25 #m). 9. Aspidorhynchus acutirostris (ICH-260.1). Lurni~re naturelle transmise. Ddtail montrant des ostdocytes isodiamdtriques (t~tes de fl~ches) et des canalicules de Williamson darts la zone la plus ancienne de la plaque basale (Echelle = 50 p.m).
110
cormus curtus, Saurostornus esocinus, Hypsocormus insignis and Euthynotus incognitus show radial structures that indicate a tendency to evolve into amioid-like scales (Schultze 1966, 1996).
Pholidophorus bechei has ganoid, lepidosteoid-type scales, a pattern confirmed in another Pholidophorus from the Upper Liassic of Normandy (Meunier & Brito in prep.). Pholidophorus bechei is corroborated as a basal taxon teleost although the whole family Pholidophoridae as well as other "pholidophoriforms" require revision (Arratia in press). A major problem in demonstrating the monophyly of the Teleostei when Mesozoic clades are included, lies in the difficulty of ascertaining the exact level of generality of the teleostean synapomorphies and in determining which are the "valid" synapomorphies. Recently, Brito (1997, in press) reviewed the aspidorhynchids and suggested, despite the many conflicting characters, retaining aspidorhynchids as basal teleosts based on, at least, one character: the presence of paired uroneurals in Vinctifer and Aspidorhynchus. Accepting this optic, we can conclude from the aspidorhynchids scales that: - Aspidorhynchids present typical ganoid, lepidosteoid scales. Aspidorhynchus species having lost the ganoin secondarily; - The odontodes found on the ganoin surface in aspidorhynchids are here interpreted as a plesiomorphic character find in "ganoid" fishes; these structures being homologous to the odontodes of the scales of extant polypterids and gars; - The bony basal plate composed of lamellar bone can give rise directly to the isopedine of elasmoid scales with augmentation a) of thickness of strata and b) probably of fibres diameter, this last one being linked with the presence of Mandl's corpuscles which are responsible of the progression of mineralization; - Structures like the canalicules of Williamson were considered as typical "holostean" features (gars plus Mesozoic taxa), however they are also find at the pholidophorid level what suggest a plesiomorphic feature within the actinopterygians; - Finally, accepting the aspidorhynchids as basal teleosts, we must hypothesise the orthogonal "plywood" as the plesiomorphic state, the presence of a helicoidal "plywood" being the synapomorphic state for more advanced teleosts; accepting this hypothesis, we must interpret the orthogonal "plywood" of perciformes (Meunier & Castanet 1982) as a feversal character. Another question arises: is the orthogonal "plywood" of aspidorhynchids homologous to the isospedine of polypterids' scales as suggested by Sire (1989, 1990), or to both isopedine and bony basal plate or to bony basal plate only? Effectively, isopedine formation is still unknown in the ganoid scales of taxa that are placed between the polypterid branch and the basal teleosts in the phylogenetical tree of Actinopterygii (Lauder & Liem 1983; Patterson 1994; Brito 1997). A c k n o w l e d g e m e n t s - We thanks C. Weber and M. Lemoine for technical assistance, and Mrs. V.G. da Silva and D. Martill for comenting various drafts of this work. P.M.B. examined different collections of aspidorhynchids over the last seven years
and acknowledge t h e help of m a n y curators, specially Prof. R. Billard and Dr. S. Wenz (Paris), Prof. G. A r r a t i a (Berlin), Dr. J. Tyler (Washington, D.C.), and Dr. G. Viohl (Eichstfitt). Mr. Steve Etches and Dr. D. Martill provided s a m p l e s from the Callovian and K i m m e r i d g i a n of England. P.M. B, is finantially supported by the CNPq, Brazilian Federal Government.
REFERENCES AGASSIZL. 1833-1844 - Recherches sur les Poissons fossiles. 5 vols., 1420 p., avec suppl6ment, Neuch~tel. ARAMBOURG C. & BERTIN L. 1958 - Super-Ordre des Holost6ens et des Hal6costomes (Holostei et Halecostomi). In GRASSE P.P. (ed.), Traitd de Zoologie, 13, 3: 2173-2203. Masson & Cie, Paris. AR~TL~ G. (in press) - The monophyly of teleostei and stem group teleosts. Consensus and disagreements. In ARRATIA G. & SCHULTZE H.P. (eds), Mesozoic fishes - Systematics and The Fossil Record, M6nchen (Verlag Dr. F. Pfeil). BEaG L.S. 1940 - Classification of fishes, both recent and fossils. Trudy zoologicestogo Instituta Leningrad, 5: 87-517. BRITO P.M. 1988 - La structure du suspensorium de Vinctifer, poisson actinopt6rygien m6sozoique: remarques sur les implications phylog6n6tiques. Geobios, 21: 819-823. ..... 1992 - L'endocr~ne et le moulage endocr~nien de Vinctifer comptoni (Actinopterygii-Aspidorhynchiformes) du Cr6tac6 inf~rieur du Br6sil. Annales de Paldontologie (VertdbrdsInvertdbrds), 78: 129-157. ..... 1995 - R6vision des Aspidorhynchidae (Pisces, Actinopterygii) du M6sozoYque: ost6ologie et relations phylog6n6tiques. Th6se de Doctorat, Mus6um national d'Histoire naturelle, Paris. 188 p., (in6dit). ..... 1997 - R6vision des Aspidorhynchidae (Pisces, Actinopterygii) du M6sozoique: ost6ologie, relations phylog6n6tiques, donn6es environnementales et biog6ographiques. Geodiversitas, 19: 681-772. ..... (in press) - The caudal skeleton of aspidorhynchids (Actinopterygii: Halecostomi): phylogenetic implications. In ARRATIAG. & SCHULTZEH.P. (eds), Mesozoic fishes - Systematics and The Fossil Record, Verlag Dr. F. Pfeil, Mtinchen. DE PINNAM.C.C. 1996 - Teleostean Monophyly. In M.L.J. STIASSNY, L.R. PARENTI & G.D. JOHNSOn (eds), Interrelationships of Fishes: 147-162. FRANCILLON-VIEILLOT H., BUFFRI~NIL V. DE, CASTANET J., GERAUDIE J., MEUNIER F.J., SIRE J.Y., ZYLBERBERGL. & RICQLESA. de 1990 Microstructure and mineralization of Vertebrate skeletal tissues. In J.G. CARTER(ed.), Skeletal biomineralization: patterns, processes and evolutionary trends, 1: 471-530, Van Nostrand Reinhold, New-York. CAWT M. & MEUNIER F.J. 1986 - Apport de l'6tude de l'ornemenration microscopique de la ganoine dans la d6termination de l'apparence g6n6rique et/ou sp6cifique des 6cailles isol6es. Comptes Rendus de l'Acaddmie des Sciences de Paris, 2, 363: 1259-1261. GEr~UDIE J. 1988. - Fine structural peculiarities of the pectoral fin dermoskeleton of two Brachiopterygii, Polypterus senegalus and Calamoichthys calabaricus (Pisces, osteichthyes). Anatomical Record, 221: 455-468. GIRAUD M.M., CASTANET J., MEUNIER F.J. & BOULIGAND Y. 1978 - The fibrous structure of coelacanth scales: a twisted "plywood". Tissue and Cell, 10: 671-686. GOODRICH E.S. 1907 - On the scales offish, living and extinct, and their importance in classification. Proceedings of the Zoological Society of London, 2: 751-774. HERTWIG O. 1879. - Ueber das Hautskelett der Fische. Morphologisches Jahrbuch, 5, 21 p. LAUDER G.V. & LIEM K.F. 1983 - The evolution and interrelationships of the actinopterygian fishes. Bulletin of the Museum of Comparative Zoology, 150: 95-197. MAISEYJ. G. 1991 - Vinctifer. In J.G. MAISEY(ed.), Santana Fossils, 170-189, New York, TFP. MATRAJT H., BORDIER P., MARTIN J. & HIOCO D. 1967 - Technique pour l'inclusion de biopsies osseuses non d6calcifi6es. Journal de Microscopie, 6: 499-504. MEUNIER F.J. 1980 - Les relations isop6dine-tissu osseux dans le post-temporal et les 6cailles de la ligne lat6rale de Latimeria ehalumnae (SMITH).Zoologica Scripta, 9: 307-317. ..... 1983 - Les tissus osseux des ost6ichthyens. Structure, gen6se, croissance et 6volution. Archives et Documents,
111
Micro-Edition, Institut Ethnologique, Musgum national d'Histoire naturelIe, SN, 82-600-328. ..... 1984 - Spatial organization a n d m i n e r a l i z a t i o n of t h e b a s a l plate of elasmoid scales in osteichthyans. American Zoologist, 24: 953-964. ..... 1987.- Os cellulaire, os acellulaire et t i s s u s d@rivds chez les ost~ichthyens: les p h ~ n o m ~ n e s de l'acellularisation et de la perte de min~ralisation. L'Annde Biologique, 26: 201-233. ..... & CASTANETJ. 1982 - O r g a n i s a t i o n spatiale des fibres de collag~ne de la plaque b a s a l e des 6cailles des %l@ost~ens. Zoologica Scripta, 11: 141-153. ..... & FRANCois Y. 1980 - U o r g a n i s a t i o n spatiale des fibres collag~nes et la min~ralisation des ~cailles des d i p n e u s t e s actuels. Bulletin de la Socidtd zoologique de France, 105: 215226. ..... , FRANQOISY. & CASTANETJ. 1978- ]~tude histologique et microradiographique des @cailles de quelques actinopt@rygiens primitifs actuels. Bulletin de la Socidtd zoologique de France, 103: 309-318. ..... , GAYET M., G~RAUDIE J., SIRX J.Y. & ZYLBEasERa L. 1987 Donn~es u l t r a s t r u c t u r a l e s s u r la ganoYne du d e r m o s q u e l e t t e des actinopt@rygiens primitifs. In RUSSELL D.E., SANTOROJ.-P. & SIGOGNEAu-RusSELLD. (eds), Teeth revisited, Proceedings of t h e VIIth Inter. Syrup. on D e n t a l Morphology, Paris 1986. Mgmoires du Musdum national d'Histoire natureIle, C 53: 7783. & POPLIN C. 1995 - Paleohistological s t u d y of t h e scales of Amia robusta PRIEM, 1901, Amiidae from t h e T h a n e t i a n (Paleocene) of C e r n a y (France). Geobios, M@m. sp. 19: 39-43. ..... & ZYLBER~ERGL. 1999 - The s t r u c t u r e of t h e external layer a n d of t h e odontodes of scales in Latimeria chalumnae (Sarcopterygii, Actinistia, Coelacanthidae) revisited u s i n g scann i n g a n d t r a n s m i s s i o n electron microscopy. In SERET B. & SIRE J.-Y. (eds), Proceedings of the 5th Indo-Pacific Fish Conference, Noumga, 1997, Soci~t@ FranCaise d'Ichtyologie, Paris. NICHOLSON H.A. & LYDEKKERR. 1889 - A manual ofpalaeontology. 2nd. ed., 1624 p. E d i n b u r g h a n d London. NICK~RSON W.S. 1893 - T h e d e v e l o p m e n t of t h e scales of Lepidosteus. Bulletin of the Museum of Comparative Zoology, 24: 115-139. PATTERSON C. 1973 - I n t e r r e l a t i o n s h i p s of holosteans. In GREENWOODP.M., WILES R.S. & C. PATTERSON(eds), Interelationships of fishes: 233-305. Academic Press, London. ..... 1977 - The contribution of paleontology to Teleostean phylogeny. In M.K. HECHT, P.C. GOODY & B.M. HECHT (eds), Major patterns in Vertebrate evolution: 579-643, New York. ..... 1994 - Bony fishes. In D.R. PROTHERO & R.M. SCHOCH (eds), .
.
.
.
.
Major patterns in Vertebrate evolution, Short Courses Paleontology, 7: 57-84. Paleontological Society, Tennessee. & ROSEN D. 1977 - Review of Ichthyodectiform a n d other Mesozoic teleost fishes a n d t h e theory a n d practice of classifying fossils. Bulletin of the American Museum of Natural History, 158 : 81-172. RICQLES A. DE, MEUNmR F.J., CASTANETJ. & FRANClLLON-VIEILLOTH. 1991 - Comparative m i c r o s t r u c t u r e of bone. In B.K. HALL (ed.), Bone, 3, 77 p. CRC Press, Boca Raton. SAINT-SEINE P. 1949 - Les poissons des calcaires lltographiques de Cerin (Ain). Nouvelles Archives du Musdum d'Histoire naturelle de Lyon, 2, 357 p. SANTOS R. SILVA DA 1985 - Nova caracterizagao do g6nero Vinctifer JORDAN, 1919. In ColetSnia de trabalhos paleontologicos, D e p a r t a m e n t o NacionaI de Produ~ao Mineral: 151-154, Brasilia. SCHONB(~RNERA.A., MEUNIER F.J. & CASTANETg. 1981 - The fine s t r u c t u r e of calcified Mandl's corpuscles in teleosts fish scales. Tissue and Cell, 13: 589-597. .
.
.
.
.
SCHULWZE H.-P. 1966 - M o r p h o l o g i s c h e u n d h i s t o l o g i s c h e U n t e r s u c h u n g e n a n S c h u p p e n mesozoischer actinopterygier (Obergang yon Ganoid- zu R u n d s c h u p p e n ) . Neues Jahrbuch fiir Geologie und Paliiontologie, 126: 232-314. ..... 1977 - A u s g a n s f o r m u n d E n t w i c k l u n g der r h o m b i s c h e n S c h u p p e n der Osteichthyes (Pisces). Paliiontologische Zeitschrift, 51: 152-168. ..... 1996 - The scales of Mesozoic actinopterygians. In ARRATI*G. & G. VIOL (eds), Mesozoic fishes - Systematics and Paleoecology: 83-93. Verlag Dr. F. Pfeil, M u n c h e n . ..... & STOHR D. 1996 - Vinctifer (Pisces, Aspidorhynchidae) a u s der U n t e r k r e i d e (oberes Aptium) yon Kolumbien. Neues Jahrbuch f~r Geologie und Pal(tontologie, 199: 395-415. SIRE J.Y. 1989 - Scales in y o u n g Polypterus senegaIus are elasmold: new phylogenetic implications. American Journal of Anatomy, 186: 315-323. ..... 1990 - From ganoid to elasmoid scales in t h e actinopterygian fishes. Netherland Journal of Zoology, 40: 75-92. ..... 1994 - Light and T E M s t u d y of n o n r e g e n e r a t e d a n d experim e n t a l l y r e g e n e r a t e d scales ofLepisosteus oculatus (Holostei) with particular attention to ganoYne formation. Anatomical Record, 240: 189-207. ..... , GI~RAUDIEJ., MEUNIER F.J. & ZYLBERBERGL. 1987 - On the origin of ganoine: histological a n d u l t r a s t r u c t u r a l d a t a on t h e e x p e r i m e n t a l regeneration of t h e scales of Calamoichthys ealabaricus (Osteichthyes, Brachyopterygii, Polypteridae). American Journal of Anatomy, 180: 391-402. • MEUNIER F.J. 1994 - The canaliculi of Williamson in holost e a n bone (Osteichthyes, Actinopterygii): a s t r u c t u r a l a n d u l t r a s t r u c t u r a l study. Acta Zoologica, 75: 235-247. WEiss R.E. & WATABEN. 1979 - Studies on t h e biology o f f i s h bone. III- U l t r a s t r u c t u r e of osteogenesis a n d resorption in osteocytic (cellular) a n d anosteocytic (acellular) bones. Calcified Tissue International, 28: 43-56. WOODWARDSA.S. 1895 - Catalogue of fossil fishes in the British Museum, Pt. 3. xiii + 544 p, London. ZYLBERBERGL., GERAUDIEJ., MEUNIER F.J. & SIRE J.Y. 1992 - Biomineralization in t h e i n t e g u m e n t a l skeleton of the living lower Vertebrates. In I4~LL B.K. (ed.), Bone, 4: 171-224, CRC Press. ..... , SIRE J.Y. & N~'~cI A. 1997 - Detection of amelogenin-like proteins in t h e ganoine of experimentally r e g e n e r a t i n g scales of Calamoichthys calabaricus, a primitive actinopterygian fish. Anatomical Record, 249: 86-95. .
.
.
.
.
P.M. B R I T O D e p a r t a m e n t o de Biologia A n i m a l e Vegetal U n i v e r s i d a d e do E s t a d o do Rio de J a n e i r o r u a Sao F r a n c i s c o Xavier 524 Rio de J a n e i r o , Brazil et L a b o r a t o i r e d'Ichtyologie g~ndrale et appliqu4e M u s 6 u m n a t i o n a l d'Histoire n a t u r e l l e 43 r u e C u v i e r F-75231 P a r i s cedex 05 F.J. M E U N I E R C N R S 1451, L a b o r a t o i r e d'Ichtyologie g@n~rale et appliqu@e M u s 6 u m n a t i o n a l d'Histoire n a t u r e l l e 43 r u e C u v i e r F-75231 P a r i s cedex 05 et U M A C N R S 8560, L a b o r a t o i r e d ' A n a t o m i e compar~e U n i v e r s i t ~ D. D i d e r o t 2 place J u s s i e u F-75251 P a r i s cedex 05