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Visceral Anatomy of Ocean Sunfish

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Visceral Anatomy of Ocean Sunfish This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy C. R. Biologies 335 (2012) 744–752 Contents lists available at SciVerse ScienceDirect Comptes Rendus Biologies w ww.sciencedirect.com Biodiversity/Biodiversite´ Visceral anatomy of ocean sunfish (Mola mola (L., 1758), Molidae, Tetraodontiformes) and angler (Lophius piscatorius (L., 1758), Lophiidae, Lophiiformes) investigated by non-invasive imaging techniques Anatomie visce´rale du poisson lune (Mola mola (L., 1758), Molidae, Tetraodontiformes) et de la baudroie (Lophius piscatorius (L., 1758), Lophiidae, Lophiiformes) e´tudie´e par les techniques non invasives d’imagerie a, b c d Bruno Chanet *, Claude Guintard , Thierry Boisgard , Marion Fusellier , e b d e Ce´dric Tavernier , Eric Betti , Ste´phane Madec , Yvan Richaudeau , d a a Christian Raphae¨l , Agne`s Dettaı¨ , Guillaume Lecointre a E´quipe phyloge´nie, UMR 7138 CNRS-IRD-MNHN-P6, de´partement syste´matique et e´volution, Muse´um national d’histoire naturelle, CP26, 57, rue Cuvier, 75231 Paris cedex 05, France b Laboratoire d’anatomie compare´e, ONIRIS – E´cole nationale ve´te´rinaire de l’agroalimentaire et de l’alimentation, Nantes atlantique, route de Gachet, BP 40 706, 44307 Nantes cedex 03, France c Muse´um d’histoire naturelle de Nantes, 12, rue Voltaire, 44000 Nantes, France d Unite´ d’imagerie me´dicale, ONIRIS – E´cole nationale ve´te´rinaire de l’agroalimentaire et de l’alimentation, Nantes atlantique, route de Gachet, BP 40706, 44307 Nantes cedex 03, France e SARL Image-Et, ZA des Hautes Fontenelles, 7, rue de Vince´, 35310 Mordelles, France A R T I C L E I N F O A B S T R A C T Article history: The purpose of this work is to examine the gross visceral anatomy of ocean sunfish and Received 31 January 2012 angler using non-invasive imaging techniques: computed tomography imaging (CT) and Accepted after revision 22 November 2012 magnetic resonance imaging (MRI). Similarities and differences in the internal Available online 25 December 2012 organisation of these two species are verified. Both species lack a swimbladder and present a significant asymmetry in the hepatic lobes, an elongated bile duct terminating Keywords: close to the stomach, a compact thyroid embedded in a blood lacuna, and very reduced Gross anatomy brain and spinal cord. These observations are important in regard to the close relationships Angler between Tetraodontiformes and Lophiiformes, established by several molecular works, Ocean sunfish but not yet confirmed by morpho-anatomical data. However the occurrence of these CT imaging MRI features has to be examined in other taxa before phylogenetic hypotheses are proposed. ß 2012 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. R E´ S U M E´ ´ Mots cles : L’examen de l’organisation ge´ne´rale de l’anatomie visce´rale du poisson lune et de la Anatomie ge´ne´rale baudroie par les me´thodes non invasives d’imagerie (tomodensitome´trie et imagerie par Baudroie re´sonance magne´tique [IRM]) constitue le but de ce travail. Des ressemblances et des Poisson lune diffe´rences dans l’anatomie interne sont mises en e´vidence. Chez ces deux espe`ces, la * Corresponding author. E-mail addresses: [email protected] (B. Chanet), [email protected] (C. Guintard), [email protected] (T. Boisgard), [email protected] (M. Fusellier), [email protected] (C. Tavernier), [email protected] (E. Betti), [email protected] (S. Madec), [email protected] (Y. Richaudeau), [email protected] (C. Raphae¨l), [email protected] (A. Dettaı¨), [email protected] (G. Lecointre). 1631-0691/$ – see front matter ß 2012 Acade´mie des sciences. Published by Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.crvi.2012.11.006 Author's personal copy B. Chanet et al. / C. R. Biologies 335 (2012) 744–752 745 Tomodensitome´trie vessie natatoire est absente, les lobes he´patiques sont fortement asyme´triques, le IRM conduit cystique est long et s’ouvre a` proximite´ de l’estomac, la glande thyroı¨de est incluse dans une lacune sanguine, l’ence´phale et la moelle e´pinie`re sont tre`s re´duits. Ces observations sont importantes dans le cadre de la parente´ e´troite entre Te´traodontiformes et Lophiiformes, e´tablie par plusieurs travaux mole´culaires, mais non encore confirme´e par des donne´es morpho-anatomiques. Toutefois, la distribu- tion de ces caracte`res doit eˆtre examine´e chez d’autres espe`ces avant de les conside´rer comme des re´elles hypothe`ses phyloge´ne´tiques. ß 2012 Acade´mie des sciences. Publie´ par Elsevier Masson SAS. Tous droits re´serve´s. 1. Introduction noted, for example in the organization of the spinal cord which does not extend into the spinal canal [16–18], they Ocean sunfish (Mola mola (L., 1758), Molidae, Tetra- were regarded as very different animals [19–23]. Until odontiformes) and angler (Lophius piscatorius (L., 1758), recently, angler and ocean sunfish were considered as Lophiidae, Lophiiformes) are acanthomorph fishes differ- unrelated species in hypotheses of teleostean interrela- ing considerably in their ecology and their external tionships [19–23]. However, numerous studies on both anatomy (Fig. 1). The first is one of the heaviest marine DNA sequences (mitochondrial and nuclear genes) of vertebrates (up to 2.3 tonnes [1]), a disc-shaped, laterally Lophiiformes and Tetraodontiformes species showed that flattened pelagic fish able to dive several times each day they were closely related [24–33] and share a common from the surface to a depth of more than 100 m [1–4] while ancestor with Scatophagidae, Cepolidae and Priacanthidae the second is a smaller, ventro-dorsally flattened bottom [34,35]. Two other works [36,37] examined the problem of dweller, living at depths of 30–500 m [5–7]. Ocean sunfish the phylogenetic position of these groups. Unfortunately, are rare and cosmopolitan, while anglers are currently one of these works [36] did not include both Lophiiformes fished commercially by European fisheries. The skeletal and Tetraodontiformes and thus did not challenge or anatomy of the species of these groups has been well corroborate a close relationship between them. In the described [8–10], but the characteristics of their internal other work [37], Lophiiformes and Tetraodontiformes do organs are little studied. In classic works, organs were not appear to be closely related on the basis of five gene often removed from the abdominal cavity and studied regions (nuclear and mitochondrial), but this result is quite separately [11–16]. Although a few similarities were unique, while ten different works [24–33] conducted by different teams on various genes (17 nuclear genes and 34 mitochondrial genes) corroborate a close relationship between Lophiiformes and Tetraodontiformes. If angler is a derived lophid species [7], but occupies a basal position within the Lophiiformes [38,39], ocean sunfish is a derived tetraodontiform fish [23,28,40]. Ideally, the internal anatomy of these species should also be compared to one of more basal tetraodontiforms, such as triggerfishes (Balistidae). Unfortunately, we cannot obtain large fresh specimens of this family to conduct the comparisons in similar conditions. We took the opportunity of having access to fresh ocean sunfish to conduct CT imaging and magnetic resonance imaging (MRI) investigations and to compare the internal anatomy of the ocean sunfish and the angler. 2. Materials and methods 2.1. Specimens studied Four angler specimens ((an isolated head (Total Length) TL = 25 cm) and three whole specimens (specimen 1: TL = 32.5 cm, (Standard Length) SL = 27.6 cm; specimen 2: TL = 33 cm, SL = 28.5 cm and specimen 3: TL = 62 cm, SL = 57.3 cm)) were fished in the eastern Atlantic Ocean and purchased at the fish market auction of Concarneau (France). An ocean sunfish (TL = 142 cm, body depth without median fins = 175 cm, with the right eye punc- Fig. 1. External morphology (left lateral views) of (A) an ocean sunfish tured) was fished in the western part of the English (Mola mola, Molidae) and (B) an angler (Lophius piscatorius, Lophiidae). Scale bars indicate 20 cm. Channel by local fishermen from Granville (50, France). It Drawings from F. Dejouannet. was collected by the show aquarium of Granville and then Author's personal copy 746 B. Chanet et al. / C. R. Biologies 335 (2012) 744–752 sent to the Laboratoire d’Anatomie Compare´e, ONIRIS 2.3. Magnetic resonance imaging (Nantes, France) where it has been cast for the Muse´um d’Histoire Naturelle of Nantes (a few plastiline remains are MRI examinations were also performed on each visible on Fig. 3B). The animal was conserved frozen in the specimen. Here we used a 1 Tesla supraconductor magnet Laboratoire d’Anatomie Compare´e, ONIRIS. Median fins (Harmony Siemens). A standard body coil was employed were cut to reduce the size of the specimen for the MRI and along with a three planes localizer. The T1 (TR = 516– CT examinations. The MRI examinations were conducted 656 ms and TE = 13 ms) and T2 (TR = 3840–5170 ms and in the Unite´ d’Imagerie Me´dicale, ONIRIS, the CT imaging TE = 91–115 ms) sequences in three planes (virtual sagittal, was performed by Image-Et (Mordelles, France).
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