Swollen bones in jacks and relatives (Teleostei: Acanthomorphata: Carangidae) by Bruno Chanet (1) Abstract. – the Carangidae form one of the teleostean families having the most frequent cases of hyperostosis: these bony gall-like structures can develop in many places of their skeleton. the known cases of this condition are described and analysed in a phylogenetic context. however, the presence of these swollen bones remains for now enigmatic. Résumé. – Des os gonflés chez les carangues (Teleostei: Acanthomorphata: Carangidae). Les Carangidae forment une des familles de téléostéens où les cas d’hyperostose sont les plus fréquents : des masses osseuses arrondies, gonflées, se développent çà et là dans le squelette. Ces cas sont décrits et analysés au regard de la phylogénie du groupe. Cependant, à ce jour, la présence de ces masses osseuses atypiques reste © SFI énigmatique. Received : 16 Nov. 2017 Accepted: 18 Dec. 2017 Editor : O. Otero Key words Carangidae hyperostosis Jacks (Caranx sp.) and pompanos Material and methods Review (Trachinotus sp.) are members of the this article is essentially a review and not a direct study family Carangidae, which forms a group on specimens, with one exception. a radiograph of the head of marine, tropical and subtropical of a silver scabbard fish [Lepidopus caudatus (euphrasen acanthomorphs (nelson, 2006). While 1788), SL: 790 mm, Trichiuridae, fished off the East Atlan- dissecting, cooking or eating a carangid fish, it is not rare to tic Ocean coast] has been performed at OnIRIS (nantes, observe gall-like, inflated hard bony masses on the haemal France). the fish was placed in lateral view and imaged and neural spines, the pterygiophores and some bones of the using a Convix 30 Machine with a Universix 120 command cephalic skeleton (Figs 1, 2). In english, these structures are at 46 kV and mas at 6.4 with 17 ms. Images were developed called hyperostotic bones, or swollen bones, or even “tilly using a Fuji FCR 5000. the specimen is conserved in the bones” (named after the late tilly edinger, an enthusias- collections of the department of “anatomie Comparée” at tic student of these structures, see Konnerth, 1966; Smith- OnIRIS (nantes, France). Vaniz et al., 1995). they are the result of the phenomenon of hyperostosis, also spelled ‘hyperosteosis’ (Francillon-Vieil- What is known about hyperostosis, notably in carangids lot et al., 1990). In medicine, this term refers to a pathologi- Swollen bones, as a whole or as a part of the bone, have cal context of an abnormally high amount of primary bone been mentioned in numerous teleostean fishes (Desse et al., deposition (Francillon-Vieillot et al., 1990). however, at 1981; Gauldie and Czochanska, 1990; Meunier and Desse, least in teleostean fishes, these bony structures do not seem 1994; Smith-Vaniz et al., 1995; Smith-Vaniz et Carpenter, to affect their behaviour, health or longevity (Smith-Vaniz 2006; among others). they have the appearance of a gall, et al., 1995). although such structures have been observed such as an osseous inflated pouch (Figs 1, 2). They can be in several (38) teleostean genera (Smith-Vaniz et al., 1995), present on the skull bones, including the neurocranium, on they are far more frequent in trichiurid, carangid and sciae- the elements of the pectoral and pelvic girdles, and on the nid species (Smith-Vaniz et al., 1995; Meunier et al., 2008; axial skeleton, including on the pterygiophores (Fig. 3) and Giarratana et al., 2012). a review of these bony peculiarities the haemal and the neural spines (Figs 1, 2). within carangid species is herein presented in a phylogenetic histologically, these masses are composed of acellular framework. bone in most cases and result from activation of osteogen- esis that yields primary spongy bone directly, or after an associated remodelling (Fierstine, 1968; Desse et al., 1981; (1) ISYeB, UMR 7205 CnRS-Mnhn-UPMC-ePhe, Muséum national d’histoire naturelle, Département Systématique et Évolution, CP 50, 57 rue Cuvier 75005 Paris, France. [[email protected]] Cybium 2018, 42(1): 99-103. Swollen bones in carangids Chanet Figure 1. – Radiographs of carangid fishes exhibiting hyperostosis. A: Caranx hippos (Linnaeus, 1766); B: Alectis alexandrina (Geoffroy St. hilaire, 1817). Swollen, opaque bones with red dots are sites of hyperosto- sis, modified from Smith-Vaniz et al. (1995: 576, fig. 1). SL non indicated by these authors. Figure 2. – First dorsal-fin pterygi- ophore of two adult carangids, modi- fied from Smith-Vaniz et al. (1995: 576, fig. 2). A: Caranx latus agassiz, 1831 (non hyperostic), at left in dorsal view, at right in right lateral view. B: Caranx hippos (Linnaeus, 1766) (hyperostic), at left in dorsal view, at right in right lateral view. Scale bar = 50 mm. Gauldie and Czochanska, 1990; Meunier and Desse, 1994; Smith-Vaniz et al., 1995). they often show a spongy and full of holes structure (Kaiser, 1960; Fierstine, 1968; Desse et al., 1981; Gauldie and Czochanska, 1990). they are not pathological formations (Olsen, 1971; Desse et al., 1981; Gauldie and Czochanska, 1990) because fishes bearing these structures have entirely normal behaviour (Johnson, 1973). the composition of the swellings is not different from that of normal bones (Desse et al., 1981; Laroche et al., 1982; Gaudant et al., 2010). Carangid hyperostoses appear with Figure 3. – Hyperostic dorsal-fin pterygiophores on a radiographed increasing specimen size and are thus present in rather large head of a silver scabbard fish (Lepidopus caudatus (euphrasen, 1788), SL: 790 mm, trichiuridae). hyperostic structures are and aged individuals (Desse et al., 1981; Gaudant et al., marked by red dots. Scale bar = 50 mm. 2010). Because the skeleton of the Carangidae is composed Coryphaenidae, Rachycentridae, echeneidae, Polynemmi- of acellular bone (= anosteocytic bone: Weiss and Watabe, dae and Pleuronectiformes. 1979; Meunier et al., 2008), hyperostosic structures are truly scattered islands of cellular bone in a skeleton otherwise Successive interpretations and assumptions The first illustrated case of hyperostosis in teleosts seems characterized by acellular bony tissue. this makes carangid to be in a pterygiophore figured by Worm (1655: 270; Fig. 4), hyperostosis different from that encountered in species such and cited by Weiler (1973). this bone was present in Ole as Euthynnus lineatus Kishinouye, 1920 (Scombridae) (e.g. Worm’s “cabinet of curiosities”. It was first incorrectly iden- Béarez et al., 2005). therefore, this scattering seems to tified and called ‘os wormiamum” (Worm, 1655), whereas occur consistently with ontogenetic development in the same Weiler (1973) identified this bone as a pterygiophore of bones in carangid species. Ephippus sp. (ephippidae). Later, Bell (1793) described hyperostosis has been observed in 22 teleostean families as tumours and probable exostoses swollen bony rounded (Smith-Vaniz et al., 1995), such as the trichiuridae (Fig. 3), masses on the pterygiophores of a species of Chaetodon in which 80% of the examined specimens were hyperostotic [this specimen was later identified as a batfish (Ephippidae) (Giarratana et al., 2012). however, it is within the Carangi- by Rayer (1843) following Cuvier and Valenciennes (1831), dae that genera affected by hyperostosis are the most fre- and the currently accepted valid attribution is Chaetodipter- quent (Smith-Vaniz et al., 1995: 574, tab. 1). this aptitude us faber (Broussonet, 1782) (eschmeyer and Fricke, 2010)]. to hyperostosis seems to be absent, or at least very rare, in Because the same structures exist in all specimens of the the closest relatives of carangids (harrington et al., 2016): same species, Bell (1793) concluded that these swollen bones 100 Cybium 2018, 42(1) Chanet Swollen bones in carangids were a normal part of their anatomy. Less than one century ond part of his 1875 work (Gervais, 1875b) is fully dedicat- later, Gervais (1875a, b) described cases of hyperostosis in ed to hyperostoses in teleosteans, which are described both humans and animals. he illustrated (ibid: fig. 7) abnormal morphologically and histologically. ten years later, Bland- bony masses at the distal extremities of some pterygiophores Sutton (1885) referred to such structures as either bony tumours or as cases of exostoses [i.e. any formation of new of scabbard fish (Lepidopus sp., trichiuridae), similar to the bony tissue at the surface of a bone (Manuila et al., 1995)]. earliest description figured by Worm (1655; Fig. 3). The sec- all these authors examined a variety of actinopterygian species [e.g. see Meunier and herbin (2014: table 1: 38-39) for a list of species examined by Gervais, 1875a, b]. there- fore, numerous cases of hyperostoses have been described in various species distributed in teleostean fishes (Smith- Vaniz et al., 1995, tab. 1:574) and especially in acanthomor- phata (Fig. 5). as frequently mentioned by various authors, this peculiarity is often present within the members of the Carangidae, whereas its occurrence is generally more spo- radic in other families, such as the Gadidae (Bland-Sutton, 1885; Meunier et al., 2008). So far, no clear explanation has been proposed to explain the over-representation in the Carangidae (Smith-Vaniz et al., 1995). the latter authors suggest that hyperostosis may have a genetic origin (Smith- Vaniz et al., 1995). however, functional hypotheses have generally been preferred and these have been various and numerous: from aiding in fin erection, aiding in neutral buoyancy, ageing action on bone, reaction to high tempera- tures, metabolic abnormality, pathogenic phenomenon, etc., but without reliable evidence (Meunier and Desse 1986; Smith-Vaniz et al., 1995; Meunier et al., 2008; Gaudant et Figure 4. – First known illustration of a hyperostic bone: a ptery- al., 2010). giophore of Chaetodipterus faber (Broussonet, 1782), ephippi- Outside of carangids, hyperostotic structures have been dae, modified from Worm (1655: 270). No scale indicated by this author. reported in various teleostean species of the following fami- Figure 5. – Distribution of the known cases of hyperostosis in acantho- morphata. the interrelationship tree has been modified after Chanet and Meunier (2014), following data from Smith-Vaniz et al. (1995, tab. 1:574), Betancur-R et al. (2013) and Chen et al. (2014). Spade ♠ indicates the posi- tion of the Carangidae. Black squares ■ represent groups where cases of hyper- ostosis are known, while white squares  represent where no case of hyperos- tosis has been reported so far. See text for details. Cybium 2018, 42(1) 101 Swollen bones in carangids Chanet lies: Muraenesocidae, Gadidae, Merlucciidae, Cyprinodonti- BetanCUR-R. R., BROUGhtOn R.e., WILeY e.O. et al. [24 authors], 2013. - the tree of life and a new classification of dae, Veliferidae, triglinae, Platycephalidae, Centropomidae, bony fishes. PLoS Currents Tree of Life. 2013 apr 18: 1-45. 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