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Redescription and molecular characterization of two species of Pauciconfibula (Monogenea, Microcotylidae) from trachinid fishes in the Mediterranean Sea Ramla Azizi, Chahinez Bouguerche, Mario Santoro, Delphine Gey, Fadila Tazerouti, Jean-Lou Justine, Sihem Bahri To cite this version: Ramla Azizi, Chahinez Bouguerche, Mario Santoro, Delphine Gey, Fadila Tazerouti, et al.. Redescrip- tion and molecular characterization of two species of Pauciconfibula (Monogenea, Microcotylidae) from trachinid fishes in the Mediterranean Sea. Parasitology Research, Springer Verlag (Germany), 2021, 10.1007/s00436-021-07097-9. hal-03244165 HAL Id: hal-03244165 https://hal.sorbonne-universite.fr/hal-03244165 Submitted on 1 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Parasitology Research https://doi.org/10.1007/s00436-021-07097-9 FISH PARASITOLOGY - ORIGINAL PAPER Redescription and molecular characterization of two species of Pauciconfibula (Monogenea, Microcotylidae) from trachinid fishes in the Mediterranean Sea Ramla Azizi 1 & Chahinez Bouguerche2,3 & Mario Santoro4 & Delphine Gey5,6 & Fadila Tazerouti2 & Jean-Lou Justine3 & Sihem Bahri1 Received: 2 October 2020 /Accepted: 18 February 2021 # The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021 Abstract Many Pauciconfibula spp. have a long and complicated taxonomic history. The remaining unsolved taxonomic confusion in this genus is impelled by the host range and status of Pauciconfibula spp. from trachinid fishes: Pauciconfibula trachini and Pauciconfibula draconis,fromTrachinus radiatus and Trachinus draco (Trachinidae), respectively. Pauciconfibula trachini was reported on Trachinus draco,typehostofPauciconfibula draconis suggesting thus a stenoxenic specificity for the former monogenean and the occurrence of two congeneric polyopisthocotyleans on a single host. Moreover, the validity of Pauciconfibula draconis was repeatedly questioned by several authors, unjustified synonymy between the two species was proposed, and the delimitations between the two species remained unsolved. Original descriptions were also incomplete and poorly illustrated. In this study, we provide a detailed illustrated redescription of both species based on newly collected specimens of Pauciconfibula trachini and Pauciconfibula draconis collected from their type hosts from off three Mediterranean localities: Algeria, Tunisia, and Italy. Integrative taxonomy using COI sequences was applied to resolve the delimitation between Pauciconfibula trachini and P. draconis. This study provides the first DNA barcoding for members of this genus. Keywords Integrative taxonomy . Barcoding . COI . Pauciconfibula trachini . Pauciconfibula draconis . Trachinus Introduction Hargis 1965; Chisholm et al. 1991;Cantatore,Lanfranchi& Timi, 2011), which makes it a difficult case for taxonomists. The taxonomy of monogeneans is generally based on sclero- This genus includes six nominal species (Cantatore, tized structures such as spines of the genital openings. Lanfranchi & Timi, 2011): Pauciconfibula trachini (Parona Pauciconfibula Dillon & Hargis, 1965 is characterized by & Perugia, 1889) [syn.: Microcotyle trachini Parona & unarmed male and female genital openings (Dillon and Perugia, 1889] on the starry weever Trachinus radiatus Section Editor: Shokoofeh Shamsi * Chahinez Bouguerche 3 Institut Systématique Évolution Biodiversité (ISYEB), Muséum [email protected] National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP 51, Paris 75005, France 4 1 Research Unit of Integrative Biology and Evolutionary and Department of Integrative Marine Ecology, Stazione Zoologica Functional Ecology of Aquatic Systems, Faculty of Sciences of Anton Dohrn, Villa Comunale 1, 80121 Naples, Italy Tunis, Université de Tunis El Manar, Tunis, Tunisia 5 Service de Systématique Moléculaire, UMS 2700 CNRS, Muséum National d’Histoire Naturelle, Sorbonne Universités, 43 Rue Cuvier, 2 Faculté des Sciences Biologiques, Laboratoire de Biodiversité et CP 26, 75231 Paris Cedex 05, France Environnement: Interactions – Génomes, Université des Sciences et de la Technologie Houari Boumediene, BP 32, El Alia Bab Ezzouar, 6 UMR7245 MCAM, Muséum National d’Histoire Naturelle, 61, Rue Algérie, Alger, Algeria Buffon, CP52, 75231 Paris Cedex 05, France Parasitol Res Cuvier, 1829 off the Italian coast (Parona & Perugia, 1889, in an unjustified action, Radujkovic and Euzet (1989) 1890); P. draconis (Briot, 1904) [syn. : Microcotyle trachini assigned their specimens collected on T. draco to P. trachini Briot, 1904] on the greater weever T. draco Linnaeus, 1758 and synonymized the latest with P. draconis (Radujkovic and from the English Channel and off Scotland (Briot 1904;Nicoll Euzet 1989). 1914); P. pogoniae (MacCallum, 1913) on the black drum During a parasitological survey of parasites infecting Pogonias cromis (Linnaeus 1766) [syn.: M. pogoniae Mediterranean marine teleosts, some monogeneans were MacCallum, 1913] from New York, USA (MacCallum collected from the gills of two trachinids, Trachinus 1913); P. euzeti (Ktari, 1971) [syn.: Aspinatrium euzeti radiatus,andTrachinus draco. After detailed morpholog- Ktari, 1971] on the pink dentex Dentex gibbosus ical study, we identified them as Pauciconfibula trachini (Rafinesque, 1810) (Ktari 1971); and P. gallieni (Euzet and P. draconis (Microcotylidae). We provide here a de- & Ktari, 1971) [syn.: A. gallieni Euzet & Ktari, 1971] on the tailed illustrated redescription of both species based on the agujon needlefish Tylosurus acus acus (Lacépède, 1803) newly collected specimens from their type-hosts. (Euzet and Ktari 1971) off the Tunisian coast. Except Integrative taxonomy is applied herein to resolve the de- P. gallieni collected from the inner operculum of its host limitation between the two species. (Euzet and Ktari 1971), all the previously mentioned species inhabit gills of marine teleosts. In contrast, the latest species added to this genus, P. subsolana Chisholm, Beverley-Burton & McAlpine, 1991, was collected in the Saint John River, Material and methods Canada, from the gills of the white perch Morone americana (Gmelin, 1789) (Chisholm et al. 1991), a Moronidae Jordan & Collection and sampling of fish Evermann, 1896 occurring in fresh, brackish and coastal waters. From March 2014 to January 2018, a total of 558 trachinid Many Pauciconfibula spp. have a long and complicated fishes belonging to Trachinus draco (67 specimens) and taxonomic history (Table 1). First described as members of T. radiatus (491 specimens) were collected from four marine Microcotyle Van Beneden and Hesse, 1863 (Briot 1904; regions, located in the Mediterranean sea: Bay of Bizerte (37° MacCallum 1913; Parona & Perugia, 1889, 1890)orof 20′ N, 9° 53′ E), Gulf of Tunis (36° 49′ N, 10° 18′ E), Sousse Aspinatrium Yamaguti, 1963 (Euzet and Ktari 1971;Ktari (35° 50′ N, 10° 38′), and Mahdia (35° 29′ N, 11° 3′ E) along 1971), they have been placed in Bradyhaptorus Unnithan, the Tunisian coast; Bouharoun (36° 37′ N, 2° 39′ E) and 1971 (Unnithan 1971) then in Pseudaspinatrium Mamaev, Algiers (28° 01′ N, 1° 39′ E) along the Algerian coast, and 1986 (Mamaev 1986) before their inclusion in Gulf of Naples (off Capri Island, 40° 33′ N, 14° 13′ E), Pauciconfibula (Chisholm et al. 1991; Dillon and Hargis Italy. The number of examined specimens and the range of 1965). total length (TL) according to the locality are given in However, the remaining unsolved taxonomic confusion in Table 2.Fishspecimensweretransferredtothelaboratory the genus Pauciconfibula is prompted by the host range and shortly after capture and identified using keys (Fischer status of Pauciconfibula spp. from trachinid fishes: et al. 1987) and examined fresh on the day of purchase. 1. Pauciconfibula trachini was first described from Gill arches were removed, placed in separate Petri dishes, Trachinus radiatus (Bychowsky 1961; Parona 1889, 1890) and observed under a microscope for the presence of then reported on a congeneric host T. draco (Akmirza 2004; monogeneans. López-Román and Guevara Pozo 1973; Radujkovic and Euzet 1989), the type host of P. draconis. This indicates a stenoxenic specificity for P. trachini and the occurrence of Monogeneans two congeneric polyopisthocotyleans on a single host. 2. The original description of P. draconis (Briot 1904)and Morphological methods subsequent redescriptions (Nicoll 1914)wereincompletewith imprecise illustrations giving thus insufficient data for com- Monogeneans were removed from gills using fine dissection parison. Although some authors suggested the conspecificity needles, then preserved in 70% ethanol, stained with acetic of P. draconis with P. trachini (Chisholm et al. 1991;Dillon carmine, dehydrated in graded ethanol series (70, 96, and and Hargis 1965;Nicoll1914), they still listed it as a distinct 100%), cleared in clove oil, and mounted in Canada balsam. species imminent additional observation (Chisholm et al. Drawings were made with the help of
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    APPENDIX 1 Classified list of fishes mentioned in the text, with scientific and common names. ___________________________________________________________ Scientific names and classification are from Nelson (1994). Families are listed in the same order as in Nelson (1994), with species names following in alphabetical order. The common names of British fishes mostly follow Wheeler (1978). Common names of foreign fishes are taken from Froese & Pauly (2002). Species in square brackets are referred to in the text but are not found in British waters. Fishes restricted to fresh water are shown in bold type. Fishes ranging from fresh water through brackish water to the sea are underlined; this category includes diadromous fishes that regularly migrate between marine and freshwater environments, spawning either in the sea (catadromous fishes) or in fresh water (anadromous fishes). Not indicated are marine or freshwater fishes that occasionally venture into brackish water. Superclass Agnatha (jawless fishes) Class Myxini (hagfishes)1 Order Myxiniformes Family Myxinidae Myxine glutinosa, hagfish Class Cephalaspidomorphi (lampreys)1 Order Petromyzontiformes Family Petromyzontidae [Ichthyomyzon bdellium, Ohio lamprey] Lampetra fluviatilis, lampern, river lamprey Lampetra planeri, brook lamprey [Lampetra tridentata, Pacific lamprey] Lethenteron camtschaticum, Arctic lamprey] [Lethenteron zanandreai, Po brook lamprey] Petromyzon marinus, lamprey Superclass Gnathostomata (fishes with jaws) Grade Chondrichthiomorphi Class Chondrichthyes (cartilaginous
  • (Muğl ) O Ho Kly Ġġ Ġ Ġcġl

    (Muğl ) O Ho Kly Ġġ Ġ Ġcġl

    NK NĠ Ġ Ġ N ĠLĠML Ġ N Ġ OK O Ġ G LL K KÖ ĠN (MUĞL ) O HO K L Y Ġġ Ġ ĠCĠLĠĞĠ Y PIL N L K (Dicentrarchus labrax) ÇĠPU (Sparus aurata) LIKL IN ULUN N K OP Ġ L ĠN LĠ L NM Ġ Quyet PHAN VAN U NL Ġ N ĠLĠM LI ANKARA 2020 Her hakkı saklıdır Ö DOKTORA TEZI G LL K KOR Z N (MUĞLA) O SHOR KA SL R Y T ŞT R C L Ğ YAPILAN L VR K (Dicentrarchus labrax) V ÇIPURA (Sparus aurata) ALIKLARIN A ULUNAN KTOPARAZ TL R N L RL NM S Quyet PHAN VAN Ankara niversitesi Fen ilimleri nstit s Su r nleri Ana ilim alı anı man: Prof r Hijran YAVUZCAN u tez alı masında, G ll k Körfezinde ulunan off-shore kafeslerde yeti tiricili i yapılan levrek (Dicentrarchus labrax) ve ipura (Sparus aurata) alıklarında ulunan ektoparazitler mevsimsel olarak incelenmi tir Çalı mada 175 adet levrek ve 175 ipura olmak zere toplam 35 alık incelenmi tir alıklarda yapılan incelemeler soncunda genel parazit prevalansı levrek alıklarında %97 14, ipura alıklarında ise %5 8 olarak elirlenmi tir Levrek alıklarında tespit edilen ektoparazitlerden Diplectanum aequans, Lernanthropus kroyeri ve Amyloodinium ocellatum t rlerinin prevalansı sırasıyla %82.28, %58 85 ve %4 57 olarak elirlenmi tir Levrek alıklarında parazitlere ait ortalama bolluk de erleri; D. aequans i in 4 61± 56, L. kroyeri i in 1 33± 15 ve A. ocellatum i in 0.10± 4 olarak saptanmı tır Levrek alıklarında parazitlerin ortalama yo unlukları, D. aequans i in 5 61± 56, L.