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Major discoveries on the dermal skeleton of fossil and Recent polypteriforms: a review Blackwell Science, Ltd

Jacques Daget1, Mireille Gayet2, François J Meunier1,3 & Jean-Yves Sire3 1

Laboratoire d’Ichtyologie générale et appliquée, FR CNRS 1541, Muséum national d’Histoire naturelle, 43 rue Cuvier, 75231 Paris Cedex 05, France (e-mail: [email protected]), 2 CNRS FRE 2158, Université Claude Bernard-Lyon I, 27 boulevard du 11 novembre, 69622 Villeurbanne Cedex, France (e-mail: [email protected]), 3 CNRS UMR 8570, Université Paris 7–D. Diderot, Case 7077, 2 place Jussieu, 75251 Paris Cedex 05, France (e-mail: [email protected])

Abstract Following the discovery of the first living polypterid, Polypterus bichir, in 1802, almost two centuries later we now know of 15 living species (including four subspecies), 14 belonging to the genus Polypterus and one to the genus Erpetoichthys (Calamoichthys) all inhabiting intertropical Africa. The polypterid fossil record was for a long time reduced to some scarce, disarticulated bones, mainly scales, found in various African deposits covering a wider area than the actual geographical distribution. With the discovery, on one hand, of polypterid scales, vertebrae, dermal bones of the cranium and dorsal spiny rays in South America and, on the other hand, of scales and numerous dorsal spiny rays in Niger and Sudan, and two articulated fossils in Morocco, the story of the polypteriforms has revealed some of its mysteries. The discovery of isopedine between dentine and bony basal plate in the scales of living and fossil polypterid species is considered a synapomorphy of the group, and has been an important aid in discriminating polypterid scales from other ganoid scales. A review of the main findings during the last 20 years is presented.

Correspondence: François Meunier, Laoratoire d’Ichtyologie, MNHN, 43 rue cuvier, 75231 Paris cedex 05, France. Fax: +33 01 40 79 37 71 E-mail: [email protected]

Received 12 Aug 1999 Accepted 3 Apr 2001

Keywords: Cenozoic, Cretaceous, dorsal spines, fossils, Recent polypteriforms, scales

Introduction

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History

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The dermal skeleton of living polypteriforms

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The dermal skeleton of fossil polypteriforms

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Africa

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South America

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Conclusions

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References

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Introduction Polypteriforms (Fig. 1) or, more generally speaking, Bichirs are a small group of very peculiar osseous fish © 2001 Blackwell Science Ltd

(Nelson 1994). The variety of morphological features of polypteriforms make them a most important group, which shows a mosaic of primitive (plesiomorphic) and specialised (apomorphic) characters and, because of 113

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Figure 1 Lateral view of (A) Polypterus ansorgei, (B) Polypterus palmas and (C) Erpetoichthys calabaricus; arrows point the dorsal pinnulae (modified from Lévêque et al. 1990).

its primitive nature, the group is frequently considered in publications dealing with the relationships between fossils and recent basal actinopterygians (e.g. Patterson 1982; Gardiner 1984; Arratia and Cloutier 1996; Taverne 1996; Lund 2000). The polypteriforms were long considered as endemic to Africa where recent polypterids live and where, until recently, the only fossils were found. Recent palaeontological discoveries in both Africa and South America (Fig. 2) have provided new data modifying the story of this group. History Polypteriforms were discovered during the French expedition to Egypt conducted by General Bonaparte (1798 –1799). In 1802, Etienne Geoffroy Saint-Hilaire described the genus Polypterus and its Nilotic species, Polypterus bichir. This author wrote (Geoffroy Saint-Hilaire 1809: p. 148) ‘If I had discovered only this species in 114

Egypt, it would compensate me for the pains usually involved in a long journey. I do not know any animal more peculiar, more worthy of a naturalists’ attention and which, showing how nature can deviate from its usual standards, would be more likely to enlarge the sphere of our ideas on organisation’.1 In effect, this discovery would have received and deserved the same excitement and attention as the recent capture of a coelacanth near Sulawesi (Erdmann et al. 1998) if the media of the early 19th century had been as developed as ours nowadays. Other Polypterus species were then described, and 14 species (including four subspecies) are presently 1

English translation of the original French text. ‘Je n’aurais découvert en Egypte que cette seule espèce, qu’elle me dédommagerait des peines qu’un voyage de long cours entraîne ordinairement, car je ne connais pas d’animal plus singulier, plus digne de l’attention des naturalistes, et qui, montrant combien la nature peut s’écarter de ses types ordinaires, soit plus susceptible d’agrandir la sphère de nos idées sur l’organisation’.

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Recent

Cretaceous

Cenozoic

Holocene

Figure 2 Geographical repartition of living and fossil Polypteriformes.

valid (Poll 1942; Daget and Desoutter 1983; Gosse 1984, 1988, 1990) (Fig. 3). The related monotypic genus Calamoichthys (Smith 1866) (Erpetoichthys Smith 1865) and its type species C. calabaricus were described 63 years after Polypterus. Initially, Smith (1865) named the taxon Erpetoichthys but in a subsequent rectifying paper (Smith 1866) he changed the name to Calamoichthys in order to avoid any confusion with the Ophichthyidae Herpetoichthys (Kaup 1856). According to the rules of the International Commission of Zoological Nomenclature, Erpetoichthys is acceptable as a valid name (Art. 56 of the Code) and has priority. Until recently, polypterid fossil remains have been collected in Africa from Cenomanian (96 – 91 My) to Pliocene (5–2 My), and were mostly assigned to Polypterus sp. (Greenwood 1974, 1984; M. Gayet et al. unpublished results). For some 15 years, the study of the dermal skeleton (mainly scales and bony rays) in living species and the discovery since 1991 of new fossil remains in Africa and South America have revealed new important data (Gayet and Meunier 1991, 1996; Meunier and Gayet 1996; Gayet et al. 1997; Dutheil 1999a,b). Because these results have been published essentially in palaeontological journals, we feel that it would be interesting to review the main findings in a neontological journal more accessible to ichthyologists.

The ganoid scale of polypteriforms is close to that of Palaeonisciformes (Goodrich 1907; Aldinger 1937; Kerr 1952) as it is composed of the same three typical layers (Fig. 4): a superficial layer of ganoine covering a layer of lacunar and vascular dentine, and a deeper layer, the basal plate, made of bony tissue (Meunier 1980). However, it differs from the palaeonisciform scale in possessing a fourth layer located just below the dentine layer. The discovery of this fourth layer, isopedine (equivalent to the elasmodine of Schultze 1996), i.e. a tissue consisting of collagen fibrils organised into an orthogonal plywood-like structure (Meunier 1987), in the ganoid scales of a polypterid was important (Fig. 5A), firstly for tracing the evolution of elasmoid scales and secondly as a possible mark to distinguish polypterid scales from other ganoid scales (Sire 1989, 1990). Until this discovery, the presence of isopedine had been described in the scales of teleosts (Meunier and Castanet 1982; Meunier 1988), of Amia calva (Meunier 1981) and of living sarcopterygians (Giraud et al. 1978; Meunier and François 1980), in which the plywood-like organisation is the main character enabling identification of the elasmoid type (Meunier 1984). In juvenile Polypterus senegalus the scales are elasmoid

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Figure 3 List of living and fossil Polypteriformes.

Figure 4 Drawing of a transverse section of a polypterid scale (Erpetoichthys calabaricus). PB, basal plate; D, dermis; De, dentine; Ep, epidermis; Ga, ganoin; El, isopedine; SF, Sharpey’s fibers; WB, woven bone (modified from Sire 1995). 116

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Figure 5 (A) A 1-µm-thick longitudinal section of a scale from an adult Polypterus senegalus (EDTA demineralised; toluidine blue staining). Detail of the central region showing the four layers of the scale: ganoine (g), dentine (d), isopedine (i) and the bony basal plate (bp); e, epidermis. Scale bar, 50 µm. (B) Ground section (polarised light) of a scale of Latinopollia suarezi (ICH 24 –6; Tiupampa, Bolivia) showing the four layers: ganoine (g), dentine (d), isopedine (i) and basal plate (bp) in the central region. Resorbed areas replaced by dentine (arrows). Scale bar, 100 µm. (C) Ground section (transmitted natural light) of a scale of Latinopollia suarezi (ICH 136 – 6; Tiupampa, Bolivia) showing vascular canals and polarised osteocytes (arrow-heads) in the bony basal plate. Scale bar, 50 µm.

scales (Sire 1989). The isopedine forms first, long before the dentine, ganoine and bony layer, and it is composed of 12 –15 thin strata (c. 4 µm thick) (Fig. 5A). In each stratum the direction of the collagen fibrils (70 nm in diameter) is parallel, whereas the directions are orthogonal from one layer to the other in the successive strata (Sire 1989). Moreover, the isopedine in polypterid scales mineralises slowly and Mandl’s corpuscles are involved (Fig. 6), as they are in the basal plate of amiid and teleostean elasmoid scales (Meunier 1981; Schönbörner et al. 1981; Zylberberg et al. 1992; Meunier and Poplin 1995). In adults, isopedine is only located in the central region of the scales, between the dentine and the bony plate, and it is always present in the scales of all living polypterid species (F. J. Meunier and J.-Y. Sire, unpublished data). Because an isopedine layer, located between the dentine layer and the bony basal plate, is not known in any other types of ganoid scales described to date, in living or fossil osteichthyans, this

plywood structure with its specific localisation in the scale is considered a synapomorphy of polypteriforms (Gayet and Meunier 1992). Ganoine is acellular, devoid of collagen fibrils, and strongly mineralised (Meunier 1980). Its origin (dermal or epidermal) was long a matter of debate but, using experimental scale regeneration, Sire et al. (1986, 1987) have clearly demonstrated that ganoine is deposited by the inner epidermal cell layer. So ganoine is a true enamel (i.e. it is epidermal in origin; Meunier et al. 1987) that presents the peculiarities of being stratified and of always being covered by soft tissues, in contrast to teeth that erupt. When directly covered by the epidermis, the surface of the mature ganoine is separated from cell membranes by an unmineralised organic layer, called the intermediate layer (Zylberberg et al. 1985). A recent immunocytochemical study has shown that the organic matrix of ganoine contains amelogenin, the major protein of mammalian tooth enamel (Zylberberg et al. 1997).

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Figure 6 Scanning electron micrograph of the mineralising front of the deep face of the scale in a young (72 mm TL) Polypterus senegalus showing Mandl’s corpuscles (arrow-heads). Scale bar, 5 µm.

Polarised light has revealed that ganoine is composed of homogeneous strata separated by thin layers that appear dark in ground sections. Vascular canals perpendicular to the scale surface cross ganoine here and there, and they are connected to deeper vascular canals in the underlying dentine layer. The dentine layer is organised around denteons surrounding vascular canals that open to the surface through the ganoine. Odontoblasts underline the walls of the denteons, and their odontoblastic extensions penetrate the dentine matrix. In the lateral regions of the scale the boundary between the dentine and the bone matrix of the basal plate is not clear cut. Frequently some osteocytes are close to odontoblastic extensions in the border-line. Dentine is mineralised less than ganoine, but more than the bony plate (Meunier 1980). The basal plate is the thickest layer. It is thicker in the central part of the scale than in the periphery. It is made of superimposed lamellae of bone (called pseudolamellar bone) consisting of parallel collagen fibrils and it encloses numerous osteocytes with long and branched prolongations (Kerr 1952; Meunier 1980). The major axis of each fibril is generally parallel to the scale border. Some branched and anastomosed vascular canals, less numerous than in the dentine layer, join the deep surface of the scale to the vascular network in the dentine (Meunier 1980). More or less polarised osteocytes (Fig. 5C) are regularly arranged 118

around the lumen of these canals giving them a particular aspect. These osteocytes are similar to the polarised osteocytes described in some palaeoniscid scales like in Scanilepis (Aldinger 1937; Ørvig 1957, 1978; Schultze 1968). Growth marks, probably seasonal, are found in the basal plate of some species. A series of five successful breedings of P. senegalus has enabled the definition of developmental stages of this species by focusing on external embryonic and larval features, specially for the development of fins and squamation (Bartsch et al. 1997). The first scales to appear, at about the same time, are (i) a few lateral line scales of the pectoral region just behind the postcleithrum and (ii) a short row of caudal medio-lateral scales. The squamation then progresses: firstly along the lateral line and secondly on the dorso-lateral faces of the circumference of the body (Bartsch et al. 1997). The dermal bones of the cranium and the dorsal spines of the finlets have roughly the same structure as described above for the scales, but the ganoine is not stratified and isopedine is missing (Meunier 1980; Meinke 1982). The spines are composed of bone and dentine with their anterior part covered in ganoine. The dermal bones are ornamented with odontodes, covered by the ganoine; these odontodes are distinctly separated; they are much closer to each other on the spines where the ganoine of the more recently deposited odontodes can overlap the ganoine of older odontodes, producing what is called an odontocomplex (Ørvig 1977; Meunier 1980; Meinke 1982). At the surface of the ganoine (on scales as well as on spines or on lepidotrichia), scanning electron microscopy (SEM) has revealed the presence of numerous small, rounded reliefs (Fig. 7A), called tubercles (Schultze 1966; Ermin et al. 1971; Gayet and Meunier 1986; Meunier et al. 1987; Géraudie 1988). The diameter of these tubercles (2.19–3.20 µm) and the distances between them (5.57– 8.54 µm) are similar in all the living polypterid species examined so far (Gayet and Meunier 1986; Meunier et al. 1987), even in regenerated scales (Sire et al. 1987). Comparisons between the diameter of the tubercles and the spaces separating them enable the differentiation of polypteriform scales from those of semionotiforms and lepisosteiforms with which they can present some external similarities (Gayet and Meunier 1986, 1993). According to Komagata et al. (1993) there can be differences between tubercles of male and female of P. senegalus and Erpetoichthys calabaricus, © 2001 Blackwell Science Ltd, FISH and FISHERIES, 2, 113–124

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The dermal skeleton of fossil polypteriforms The rhomboid scales of ganoid type are broadly speaking well preserved, whatever the nature and the age of the sediments in which they are found. Indeed, scales are often the only fossilised element subsisting. It is often the case in palaeontology that taxa are clearly defined by a significant part, prior to the discovery of a completely preserved animal. That explains why initial studies are undertaken in the microscopical structure of scales, on their superficial ornamentation and, occasionally, on other rather well preserved bony pieces of the dermal skeleton (Gayet et al. 1988; Gayet and Meunier 1991, 1993; Meunier and Gayet 1996). The histological structure of these scales looks very like that of extant polypterid species with the four layers described above (Fig. 5B), and the surface of their ganoine shows the typical tubercles (Fig. 7B). Africa

Figure 7 Scanning electron micrograph view of the ganoine surface showing the tubercles of the scale in a 111-mm TL Polypterus ornatipinnis (A) and in an undetermined polypterid from In Beceten (Niger) (B). Scale bars, 10 µm.

but no measurements were given to support this assertion. In fact, our personal observations on these two species do not support this statement. Extant polypteriforms possess symmetrical dorsal spines each supporting a branched lepidotrichium (Fig. 8A); these dorsal spines are more important than scale morphology for polypterid species recognition. Effectively, some morphological peculiarities of the dorsal spine morphology, mainly its articular head (Fig. 8B & C), show diagnostic characteristics to enable identification of polypteriforms at the generic and specific level, and even to distinguish between male and female (Meunier and Gayet 2000). © 2001 Blackwell Science Ltd, FISH and FISHERIES, 2, 113–124

The deposits of the Wadi Milk Formation in Sudan (Werner 1994) and of In Beceten in Niger (Moody and Sutcliff 1991), dated as Cenomanian (96 –91 My) and Coniacian-Santonian (88 –83 My) respectively, contain the richest and most diversified remains of polypteriforms (Gayet et al. 1988; Gayet and Meunier 1996; Werner and Gayet 1997). As far back as the base of Upper Cretaceous (95 My), the genus Polypterus is represented by two species: P. dageti (Gayet and Meunier 1996) from Niger and Sudan, and P. sudanensis (Werner and Gayet 1997) from Sudan only. Polypterus is accompanied by six other genera with 15 species (Figs 2 & 3) in these two localities. All these genera and species differ from one another mainly through characteristic dorsal spine morphology (Fig. 8E & F). Asymmetrical spines, that differ strongly from those of polypteriforms living at the present time, are observed in some species (Gayet and Meunier 1996; Werner and Gayet 1997). These asymmetrical spines articulate (Fig. 8D, G & H) directly in specialised scales by means of a well-developed basal process instead of a pterygophore as observed in polypterid spines (Fig. 8E & F). In contrast to the symmetrical spines that can move only in the median plane of the fish when they are erected, the asymmetrical spines can rotate on their basal scale and slope either to the right or to the left, making an angle of c. 40° with the vertical (Gayet et al. 1997), as observed for the dorsal spines in recent pinecone fishes (Monocentridae and Beryciformes). In addition to Sudan 119

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Figure 8 (A) Lateral view of a polypterid finlet (anterior to the left); (B and C) posterior views of entire finlet spines in two living polypterids: Erpetoichthys calabaricus (B) and Polypterus ornatipinnis (C); (D–H) articular heads of finlet spines: (D) posterior view of the asymmetric spine in Inbecetemia torta (Cretaceous) (E) posterior view of the symmetric spines in Polypterus ornatipinnis and (F) in Polypterus ansorgei (living) (G) latero-posterior view of the symmetric spine in Saharichthys africanus (Cretaceous), and (H) posterior view of the asymmetric spine in Inbecetemia tortissima (Cretaceous). (D, G and H) Campanian-Maastrichtian of In Beceten, Niger. Note the twisted asymmetric spines and the difference in the development of the basal processes; the left or right basal process could be more developed according to the position of the finlet spine on the back.

and Niger, two other Cretaceous localities have provided polypteriforms; these are the Cenomanian of Egypt (Stromer 1936; Schall 1984) with Polypterus sp., Polypterus? bartheli and Polypteridae gen. & sp. indet. of Morocco (Sereno et al. 1996). In this latter locality, in addition to Bartschichthys and Sudania (Dutheil 1999a), Serenoichthys kemkemensis Dutheil 1999a (called Polypterus sp. by Dutheil 1999b) is the only known articulated fossil cladistian, but the head is lacking. Even though they are very small, the two specimens of S. kemkemensis are considered adults. They possess 13 dorsal finlets (Dutheil 1999a) but neither the morphology of the articulated head of the dorsal spiny rays nor the scale morphology and histology have been studied until now to assess their relationship with other polypteriforms. Complete skulls have recently been found by this latter author and are under study. Other younger fossil remains of polypteriforms 120

have been reported in Africa: Polypterus sp. from the Miocene of Kenya (Greenwood 1951) and Tunisia (Greenwood 1973), P. bichir ornatus (Arambourg 1948) from the Pleistocene of the Omo Valley in Turkana (Ethiopia), and Polypterus sp. from the Pleistocene of Wadi Natrum in Egypt (Greenwood 1972) and from the Holocene of the Taoudenni-Araouane Basin in Mali (Van Neer and Gayet 1988). Until now, no fossil could be assigned to the genus Erpetoichthys; all these remains are reported, because of their morphology and histology, to Polypterus sp. or to recent polypterid species. South America In Bolivia, fossil deposits of Pajcha Pata and Vila Vila (Maastrichtian), and of Tiupampa and Criadero de Loro (early late Palaeocene) have provided scales, dermal bones of crania, scapular girdles, vertebrae © 2001 Blackwell Science Ltd, FISH and FISHERIES, 2, 113–124

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and dorsal spines which were assigned with certainty to polypteriforms with regard to both their morphology and their histology (Gayet and Meunier 1991, 1993). These remains were referred to a new genus and a new species of polypterids, Dagetella sudamericana (Gayet and Meunier 1992). More recently, another genus and species, Latinopollia suarezi (Meunier and Gayet 1996, 1998) were described from the same Bolivian deposits as well as from Brasilian deposit of Acre (Maastrichtian/Palaeocene). All the scales are smooth (no ridges) as in most polypterid scales. The histology of Dagetella scales looks like similar to fossil and Recent African polypterid scales, whereas those of Latinopollia (Fig. 5B) differ slightly with the vascular canals of the basal plate surrounded by typical polarised osteocytes (Fig. 5C) that look alike those of scales in the fossil Scanilepis (Ørvig 1978). Scales of Latinopollia show a smaller number of vascular canals crossing the ganoine and more numerous and longer odontoblast canaliculi in the dentine, so that Latinopollia could belong to another unknown family of polypteriforms rather than to Polypteridae to which are, at present, assigned all the extant and fossil forms described including Dagetella (Meunier and Gayet 1996). Living polypteriforms are primary freshwater fish (sensu Myers 1949). Fossil polypteriforms of Cretaceous age are supposed to have been freshwater fish like the living ones; recent geochemical analyses confirm this for the South American taxa (Dromart et al. 1999). In the Palaeocene, polypteriform remains were components of a freshwater fish fauna (Gayet and Meunier 1998) and components of a strictly continental fauna with amphibians, snakes, turtles, crocodiles and mammals (Marshall et al. 1985). So, the presence of fossil polypteriforms in South America supports the assumption of a Gondwanian origin for the group and, accordingly, a presence previous to the splitting the African and South American continents, dated as Albian (≈ 110 My). In Australia, no dermal skeletal elements that could be assigned to polypteriforms have been found in the Cretaceous-Tertiary formations to date. In India, all ganoid scales from levels of the same age are of the lepisosteoid type, i.e. characterised by the presence of Williamson’s canaliculi and the lack of dentine (F. J. Meunier and M. Gayet, unpublished data). The absence of polypteriforms in these two continents (even if not proof ) makes it possible to place the diversification of this group between 148 million years (age of the split between India and Africa) and 110 million years (age of the split between Africa and South America).

The current studies of fossil polypteriforms can still produce surprises. The polypteriforms as a Gondwanian group can be divided into African and South American species. During the Upper Cretaceous period, these fishes were broadly diversified in Africa and at that time comprised many genera and species. Because of its explosive appearance in the Cenomanian period, the group seems to have originated at that time. There is no anatomical intermediate structure present either in their supposed ancestral group or in any other group. Phylogenetic innovations or strong potential of fossilisation could explain this phenomenon of diversification (Gayet et al. 2001). Most polypteriform genera disappeared before Santonian time. Dagetella and Latinopollia passed the K/T boundary and quickly disappeared thereafter, whereas Polypterus has a continuous African record through to the present, and now shows another obvious specific diversification; the second living genus Erpetoichthys is of more recent emergence. No polypterid is living in South America today. The phylogeny of polypteriforms is complicated and still under debate. There is a consensus about the placement of Cladistia inside Actynopterygii. However, according to some authors (Aldinger 1937 and Schultze 1968; both working on scales; Selezneva 1985 and Sytchevskaya 1999, working on complete fish), they could be related to neopterygian taxa, while for others (Patterson 1982; Gardiner 1984; Arratia and Cloutier 1996; Taverne 1996; Lund 2000), they are the sister-group of Actinopteri (i.e. Recent Actinopterygii). Phylogeny is not the subject of this paper mainly because the morphology and structure of polypteriform scales and spines, which are apomorphies of the group, cannot support any phylogenetical assignment. Whatever is true, these two statements imply a far greater antiquity for the polypterid lineage (Trias for the former, if neopterygians, and Middle Devonian for the later, if a sistergroup of Actinopteri) than that demonstrated by the fossil records. The appearance of polypteriforms in Cretaceous time could only indicate that either the proposed phylogeny is wrong or the fossil record is strongly incomplete. According to Liem (1973) ‘adaptative radiation will not occur until after evolutionary novelty has reached a certain degree of development’. Regarding this statement, polypteriforms could have been present, but unrecognisable, before Cenomanian. This review underlines the important contribution of comparative studies in living species to our

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knowledge of the polypteriforms (F. J. Meunier and M. Gayet, unpublished results). The discovery of isopedine in the scales and of the typical morphology of the articular head of the dorsal spines in living polypterids have been of considerable help in the identification of fossil polypteriform remains in South American deposits and in the recognition of the diversification of this group during the Upper Cretaceous period. References Aldinger, H. (1937) Permische Ganoidfische aus Ostgrönland. Meddelelser om Grønland 102, 1– 392. Arambourg, C. (1948) Contribution à l’étude géologique et paléontologique du bassin du lac Rodolphe et de la basse vallée de l’Omo. Miss. scient. Omo. Géologie, Paléontologie. Firmin Didot, Paris, 1562 pp. Arratia, G. and Cloutier, R. (1996) Reassessment of the morphology of Cheirolepis canadensis (Actinopterygii). In: Devonian Fishes and Plants of Miguasha Quebec, Canada (eds H.-P. Schultze and R. Cloutier). Verlag Dr. F. Pfeil, München, pp. 165 –197. Bartsch, P., Gemballa, S. and Piotrowski, T. (1997) The embryonic and larval development of Polypterus senegalus Cuvier, 1829: its staging with reference to external and skeletal features, behaviour and locomotory habits. Acta Zoologica 78, 309 –328. Daget, J. and Desoutter, M. (1983) Essai de classification cladistique des Polyptéridés (Pisces, Brachiopterygii). Bulletin du Muséum National d’Histoire Naturelle, Paris 4e, Série 5, 661–674. Dromart, G., Lécuyer, C., Gayet, M., Granjean, P., Méon, H. and Otero, O. (1999) Reconstructing aquatic environments and climate in the Maastrichtian-Danian of Bolivia by combining sedimentology, palynology, and δ 18O of vertebrates. In: 6th Symposium of the European Union of Geosciences (March 28–April 1, Strasbourg, France). Journal of inference abstract, 4 (1999), p. 210. Dutheil, D.B. (1999a) The first articulated fossil cladistian: Serenoichthys kemkemensis, gen. et sp. nov., (Actinopterygii: Cladistia) from the Cretaceous of Morocco. Journal of Vertebrate Paleontology, 19, 243 –246. Dutheil, D.B. (1999b) Freshwater fish fauna from the Upper Cretaceous of Morocco. In: Mesozoic Fishes 2. Systematics and Fossil Record (eds G. Arratia and H.P. Schultze). Verlag Dr. F. Pfeil, München, pp. 553 –564. Erdmann, M.V., Caldwell, R.L. and Moosa, M.K. (1998) Indonesian ‘king of the sea’ discovered. Nature 395, 335. Ermin, R., Rau, R. and Reibedanz, H. (1971) Der submikroskopische Aufbau der Ganoidschuppen von Polypterus im Vergleich zu den Zahngeweben der Säugetiere. Biomineralisation 3, 312 –321. Gardiner, B.C. (1984) The relationships of the palaeoniscid fishes, a review based on new specimens of Mimia and Moythomasia from the Upper Devonian of Western

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