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(Monogenea : Ancyrocephalidae) from Mugil Cephalus

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(Monogenea : Ancyrocephalidae) from Mugil Cephalus Ahead of print online version FoliA PArAsitologicA 60 [5]: 433–440, 2013 © institute of Parasitology, Biology centre Ascr issN 0015-5683 (print), issN 1803-6465 (online) http://folia.paru.cas.cz/ Ligophorus species (Monogenea: Ancyrocephalidae) from Mugil cephalus (Teleostei: Mugilidae) off Morocco with the description of a new species and remarks about the use of Ligophorus spp. as biological markers of host populations Fouzia El Hafidi1, Ouafae Berrada Rkhami2, Isaure de Buron3, Jean-Dominique Durand4 and Antoine Pariselle5 1 Département de Biologie, Université Hassan ii, Faculté des sciences et techniques de Mohammedia, Mohammedia, Morocco; 2 Laboratoire de Zoologie et de Biologie générale, Université Mohammed V – Agdal, Faculté des sciences, rabat, Morocco; 3 Department of Biology, college of charleston, charleston, UsA; 4 Institut de recherche pour le développement (irD), Université Montpellier, Montpellier, France; 5 Institut de recherche pour le développement (irD), isE-M, Université Montpellier, Montpellier, France Abstract: gill monogenean species of Ligophorus Euzet et suriano, 1977 were studied from the teleost Mugil cephalus linneaus (Mugilidae) from the Mediterranean and Atlantic coasts of Morocco. We report the presence of L. mediterraneus from both the Mediterranean and Atlantic coast and L. cephali and L. maroccanus sp. n. from the Atlantic coast only. the latter species, which is described herein as new, resembles L. guanduensis but differs from this species mainly in having a shorter penis compared to the accessory piece, a proportionally longer extremity of the accessory piece and a less developed heel. the utility of Ligophorus spp. as markers of cryptic species of the complex M. cephalus is discussed in the context of species diversity and geographical distribution of these monogeneans on this host around the world. Presence of different species of Ligophorus on M. cephalus sensu stricto from the Atlantic and Mediterranean coast of Morocco demonstrates the usefulness of these species as fine resolution markers of genetic populations of their host, which are known to inhabit those coasts. Keywords: Ligophorus maroccanus sp. n., cryptic species marker, geographical distribution, Atlantic ocean, Mediterranean sea Ligophorus Euzet et suriano, 1977 (Monogenea) be- sea (Paperna and overstreet 1981), Malacca strait (soo longs to the Ancyrocephalidae Bychowsky, 1937. Euzet and lim 2012) and the East and south china seas (Zhang and suriano (1977) erected this genus with the type spe- and Ji 1981, Pan 1999, Zhang et al. 2001, 2003). today, cies L. vanbenedenii (Parona et Perugia, 1890) to describe there are 50 species of Ligophorus parasitising different parasites from gills of mugilids in the Mediterranean sea. species of mugilids and 17 of these are found on species Euzet and suriano (1977) described 11 species of Ligo- making up the flathead mullet Mugil cephalus linnaeus phorus, of which nine were new to science, all previously complex (see below). known as Ancyrocephalus vanbenedenii Parona et Peru- Whereas M. cephalus was first described in the Medi- gia, 1890. terranean sea off the coasts of Egypt, this species was since 1977, numerous species of Ligophorus have later considered cosmopolitan. recent genetic investiga- been described from different mugilid hosts around the tions on geographical populations of M. cephalus dem- world, which are generally specific of their host: from the onstrate the presence of cryptic species (shen et al. 2011, Mediterranean sea (Euzet and sanfilippo 1983, D’Amelio Durand et al. 2012), phylogenetic relationships of which et al. 1996), Black sea (sarabeev and Balbuena 2004, remain largely unknown (Whitfield et al. 2012). sarabeev et al. 2005, Balbuena et al. 2006, rubtsova et in Morocco, the split of the coasts by the strait of gi- al. 2006, Dmitrieva et al. 2007), Pacific ocean (Fernan- braltar (Fig. 1) was shown to lead to the presence of ge- dez 1987), Atlantic ocean (Fuentes and Nasir 1990, Ab- netically differentiated populations of the Mediterranean dallah et al. 2009, Faila siquier and ostrowski de Núñez M. cephalus referred hereafter as M. cephalus sensu stric- 2009, Marcotegui and Martorelli 2009), Yellow sea (Hu to (s.s.) on the Mediterranean and Atlantic coasts (Durand and li 1992), sea of Japan (rubtsova et al. 2007), red et al. 2013). Address for correspondence: A. Pariselle, Ur 203/UMr 5554, isE-M, Université Montpellier ii, cc 063, 34095 Montpellier cedex 5, France. Phone: +33 4 67 14 46 84; E-mail: [email protected] 433 Ahead of print online version Fig. 2. Measurements of various sclerotized organs. A – ven- tral transverse bars: l – total length, d – distance between ex- pansions; B – anchor: a – total length, b – distance shaft-point, Fig. 1. sampling localities in Morocco. c – shaft length, d – guard length, e – point length, f – blade length; C – hook; D – male copulatory organ (Mco): a – penis the monogeneans of M. cephalus are of particular in- total length, b – bipartite base length, c – accessory piece length, terest because their oioxenous nature, i.e. strict host spe- d – extremity of accessory piece length; E – vagina total length. cificity, makes them good host population markers (see Pariselle et al. 2011 for review). thus, gill monogeneans 24 hours prior to freezing upon return to the laboratory. gill such as Ligophorus spp. may help determine the assem- arches were separated and placed individually in Petri dishes. blage of cryptic species that constitute the M. cephalus Monogeneans were collected according to procedures de- sensu lato (s.l.) complex. scribed by Pariselle and Euzet (1994). Worms were mounted either in Malmberg’s (Malmberg 1957) or in Berlèse’s medium therefore, this study had two goals: firstly, to report and sealed with glyceel (see Bathes 1997). Worms were ob- previously described Ligophorus species and describe served at 400× and 1 000× using a compound microscope. ter- a new one from M. cephalus s.s. from the coast of Mo- minology and numbering of the haptor parts are those adopted rocco, and secondly to test whether the diversity of Ligo- at icoPA iV (Euzet and Prost 1981). Measurements were taken phorus spp. on Moroccan flathead mullet reflects the finer from mounted specimens using a leica 2500 compound mi- scale population structure of M. cephalus s.s. croscope equipped with a leica DFc 320 digital camera using lAs 3.1 software (Fig. 2). All measurements are in microme- MATERIALS AND METHODS tres and expressed as follows: mean ± standard deviation with minimum-maximum value and number of observations in par- specimens of Mugil cephalus s.s. (n = 120) were captured atheses. Micrographs were taken using a reichert-Jung Polyvar primarily in the lagoon of Moulay Bousselham (Atlantic ocean: compound microscope at 1 000× magnification using interfer- 34°48'-34°53'N, 6°14'-6°18'W) from December 2008 to Janu- ence phase contrast. the material was deposited at the Musée ary 2010. other specimens were captured from the Khnifiss National d’Histoire Naturelle de Paris (MNHN). lagoon (n = 30) (Atlantic ocean: 27°57'-28°03'N, 12°13'- 12°19'W) in March and september 2011 and from the Mar chica (n = 13) (Mediterranean sea: 35°06'-35°15'N, 2°45'- RESULTS 2°56'W) in January 2012. Moulay Bousselham, also known as No Ligophorus specimens were found in any of the Merja Zerga, is 35 km2, is located 120 km north of rabat and 30 flathead mullets dissected from Khnifiss lagoon. it is the northernmost lagoon on the Moroccan Atlantic coast However, L. mediterraneus was found from Moulay (Fig. 1). the Khnifiss lagoon is the most important desert wet- Bousselham and Mar chica lagoons. Ligophorus cephali land in Morocco (6 500 ha) and lies 900 km south of rabat. the and a new species, L. maroccanus sp. n., were found from Mar chica lagoon, also called Nador lagoon, is on the Medi- terranean coast and is 22 km long and 6 km wide. fish collected from Moulay Bousselham lagoon only. several species of fish, including five species of Mugilidae Ligophorus mediterraneus sarabeev, Balbuena et belonging to three genera, live in sympatry in these three eco- Euzet, 2005 Fig. 3 A,c systems: Mugil cephalus, Chelon labrosus (risso), Liza ramada (risso), L. aurata (risso) and L. saliens (risso). Fish, purchased Redescription. Body 791 ± 7 (780-800; n = 7) long from local fishermen shortly after they were captured, were and 120 ± 1 (119–121; n = 7) wide at level of ovary. identified and either dissected on site or kept on ice for about Mouth opening ventral. Pharynx ovoid, 37 ± 0.4 (37– 38; 434 Ahead of print online version El Hafidi et al.:Ligophorus spp. as markers for Mugil cephalus populations A B C D Fig. 3. A – Ligophorus mediterraneus – haptor; B – Ligophorus cephali – male copulatory organ; C – Ligophorus mediterraneus – male copulatory organ; D – Ligophorus cephali – haptoral sclerites. scale bars = 30 μm. n = 8) in diameter, followed by short oesophagus; diges- b: 10 ± 1 (8–12; n = 12) long, going through accesso- tive tract divided in two branches joined posteriorly. ry piece, c: 37 ± 4 (31–45; n = 12) long, which ends in Haptor with 14 hooks, 13 ± 0.2 (13–14; n = 7) long, rounded claw. four anchors and two transverse bars. Ventral bar slightly H o s t : Mugil cephalus linnaeus (Mugilidae). curved, thick at middle, with two median anterior expan- l o c a l i t i e s : lagoons of Moulay Bousselham (Atlantic sions close together, 41 ± 1 (38–42; n = 12) long, expan- ocean) (prevalence 90%) and Mar chica (Mediterranean sions at 10 ± 2 (7–12; n = 12) from each other. Dorsal bar sea) (prevalence 100%), Morocco. slightly arched, with rounded extremities, 40 ± 2 (34–43; s i t e : gills. n = 12) long. M a t e r i a l e x a m i n e d : 12 adult specimens mounted in Ventral and dorsal anchors similar in shape and size, Malmberg’s medium (glycerin amonium picrate, gAP).
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