Metazoan Parasites of the Mediterranean Garfish Belone belone gracilis (Teleostei: Belonidae) as a Tool for Stock Discrimination


The aim of the present study was to provide a current survey of metazoan parasites of the Mediterranean garfish Belone belone gracilis Lowe, 1839 off Tunisian coast and their potential use as biological tags for discriminate stocks. Parasitological analysis of 453 specimens of B. b. gracilis along the eastern Tunisian coast revealed the presence of ten species of metazoan parasites: one monogenean Axine belones Abildgaard, 1794; four digeneansLecithostaphylus retroflexus (Molin, 1859), Tergestia acanthocephala (Stossich, 1887) Stossich, 1899, Aponurus laguncula Looss, 1907 and Condylocotyla pilodora(metacercaria) Pearson et Prévot, 1985; one copepod Bomolochus bellonesBurmeister, 1835; two isopods Irona nana Schioedte et Meinert, 1884 andNerocila orbignyi (Guérin-Méneville, 1832); 1 acanthocephalan Telosentis exiguus (Von Linstow, 1901) and one nematod Anisakid larvae. Discriminant analysis using parasites as biological tags, allowed identifying two stocks ofB. b. gracilis. Digenea L. retroflexus, A. laguncula and Anisakid larvae were the most important species in determining the position of sampled fishes from the central coast off Tunisia. Metacercaria C. pilodora characterized specimens from the Southern coast off Tunisia. These results were corroborated by comparing parameters of prevalence and mean abundance between zones. Discriminant analysis used for the separation of B. b. gracilis between seasons in both localities showed that a seasonal variation affected mainly specimens from the center suggesting seasonal move of fishes.

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Châari, M. , Feki, M. and Neifar, L. (2015) Metazoan Parasites of the Mediterranean Garfish Belone belone gracilis (Teleostei: Belonidae) as a Tool for Stock Discrimination. Open Journal of Marine Science, 5, 324-334. doi: 10.4236/ojms.2015.53027.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Collette, B.B. (2003) Family Belonidae (Bonaparte, 1832) Needlefish. Annotated Checklist of Fish. California Academy of Sciences, 16, 22 p.
[2] Dujardin, F. (1845) Histoire naturelle des Helminthes ou Vers intestinaux. Librairie encyclopedique de Roret, Paris, 654 pp.
[3] Timon-David, J. (1937) Etude sur les trématodes parasites des poissons du golfe de Marseille. Bulletin de l’Institut Océanographique de Monaco, 717, 1-24.
[4] Vervoort, W. (1962) A Review of the Genera and Species of the Bomolochidae (Crustacea, Copepoda), Including the Description of Some Old and New Species. Zoologische Verhandelingen, 56, 1-111.
[5] Trilles, J.P. and Raibaut, A. (1971) Aegidae et Cymothoidae parasites de poissons de mer Tunisienne. Premiers résultats. Bulletin national d’océanographie et de pêche Salammb?, 2, 71-86.
[6] Euzet, L. and Lopez-Roman, R. (1973) Nuevos datos sobre la morfologia y la anatomia de Axine belones Abildgaard, 1794 (Monogenea). Revista Iberica de Parasitologia, 33, 557-571.
[7] Pearson, J.C. and Prévot, G. (1985) A Revision of the Subfamily Haplorchinae Looss, 1899 (Trematoda: Heterophyidae). III—Genera Cercarioides and Condylocotyla n.g. Systematic Parasitology, 7, 169-197.
[8] Bray, R.A. and Mackenzie, K. (1990) Aponurus laguncula Looss, 1907 (Digenea: Lecithasteridae): A Report from Herring, Clupea harengus L., in the Eastern English Channel and a Review of Its Biology. Systematic Parasitology, 15, 117-124.
[9] Cheikhrouha, C.F., Zghidi, W., Ould Yarba, L. and Trilles, J.P. (2000) Les Cymothoidae (Isopodes parasites de poissons) des c?tes tunisiennes: Ecologie et indices parasitologiques. Systematic Parasitology, 46, 143-150.
[10] Bartoli, P., Bray, R.A. and Gibson, D.I. (2003) Lecithostaphylus retroflexus (Molin, 1859) (Zoogonidae) and Tergestia acanthocephala (Stossich, 1887) (Fellodistomidae) (Digenea) from the Epipelagic Teleost Belone belone (L.) in the Western Mediterranean. Systematic Parasitology, 54, 131-143.
[11] Kvach, Y. and Sasal, P. (2010) Telosentis exiguus (von Linstow, 1901) (Palaeacanthocephala: Illiosentidae), a Generalist Parasite of Fishes in the Mediterranean Basin. Systematic Parasitology, 76, 9-18.
[12] Radujkovic, B.M. and Sundic, D. (2014) Parasitic Flatworms (Platyhelminthes: Monogenea, Digenea, Cestoda) of Fishes from the Adriatic Sea. Natura Montenegrina, 13, 7-280.
[13] Oktener, A. (2005) A Checklist of Parasitic Helminths Reported from Sixty-Five Species of Marine Fish from Turkey Including Two New Records of Monogeneans. Zootaxa, 1063, 33-52.
[14] Keser, R., Bray, R.A., Oguz, M.C., Celen, S., Erdogan, S., Dogutürk, S., Aklanoglu, G. and Marti, B. (2007) Helminth Parasites of Digestive Tract of Some Teleost Fish Caught in the Dardanelles at Canakkale, Turkey. Helminthologia, 44, 217-221.
[15] Rynkiewicz, J. (1970) The Parasite Fauna of Garfish Belone belone (L.) from Puck Bay. Acta Ichthyologica et Piscatoria, 1, 103-106.
[16] Grabda, J. (1981) Parasitic Fauna of Garfish Belone belone (L.) from the Pomeramian Bay (Southern Baltic) and Its Origin. Acta Ichthyologica et Piscatoria, 11, 75-85.
[17] Luque, J.L. and Poulin, R. (2007) Metazoan Parasite Species Richness in Neotropical Fishes: Hotspots and the Geography of Biodiversity. Parasitology, 134, 865-878.
[18] Poulin, R. (2007) The Structure of Parasite Communities in Fish Hosts: Ecology Meets Geography and Climate. Parassitologia, 49, 169-172.
[19] Timi, J.T., Lanfranchi, A.L. and Luque, J.L. (2010) Similarity in Parasite Communities of the Teleost Fish Pinguipes brasilianus in the Southwestern Atlantic: Infracommunities as a Tool to Detect Geographical Patterns. International Journal for Parasitology, 40, 243-254.
[20] Braicovich, P.E., Luque, J.L. and Timi, J.T. (2012) Geographical Patterns of Parasite Infracommunities in the Rough Scad, Trachurus Lathami Nichols, in the Southwestern Atlantic Ocean. Journal of Parasitology, 98, 768-777.
[21] Williams, H.H., MacKenzie, K. and McCarthy, A.M. (1992) Parasites as Biological Indicators of the Population Biology, Migrations, Diet, and Phylogenetics of Fish. Reviews in Fish Biology and Fisheries, 2, 144-176.
[22] MacKenzie, K. and Abaunza, P. (1998) Parasites as Biological Tags for Stock Discrimination of Marine Fish: A Guide to Procedures and Methods. Fisheries Research, 38, 45-56.
[23] MacKenzie, K. (2002) Parasites as Biological Tags in Population Studies of Marine Organisms: An Update. Parasitology, 124, 153-163.
[24] George-Nascimento, M. (2000) Geographical Variations in the Jack Mackerel Trachurus symmetricus murphyi Populations in the Southeastern Pacific Ocean as Evidenced from the Associated Parasite Communities. Journal of Parasitology, 86, 929-932.[0929:GVITJM]2.0.CO;2
[25] Oliva, M.E. (2001) Metazoan Parasites of Macruronus magellanicus from Southern Chile as Biological Tags. Journal of Fish Biology, 58, 1617-1624.
[26] Timi, J.T. (2003) Parasites of Argentine Anchovy in the Southwest Atlantic: Latitudinal Patterns and Their Use for Discrimination of Host Populations. Journal of Fish Biology, 63, 90-107.
[27] MacKenzie, K. and Abaunza, P. (2005) Parasites as Biological Tags. In: Cadrin, S.X., Friedland, K.D. and Waldman, J.R., Eds., Stock Identification Methods: Applications in Fisheries Science, Elsevier, San Diego, 211-226.
[28] Jarboui, O., Ghorbel, M. and Bouain, A. (1998) Le stock du pageot commun Pagellus erythrinus du golfe de Gabès (Tunisie): Etat d’exploitation et possibilités d’aménagement. Cahier Options Mediterranéenne, 35, 251-260.
[29] Anonymous (2002) Rapport national sur la biodiversité marine et c?tière en Tunisie. Institut National Agronomique de Tunisie.
[30] Anonymous (2010) Annuaires statistiques des produits de la pêche en Tunisie. Direction Générale de la pêche et de l’aquaculture.
[31] Bauchot, M.L. (1987) Méditerranée et mer Noire. Zone de pêche 37. In: Fisher, W., Bauchot, M.L. and Scheinder, M., Eds., Fiches FAO d’Identification des Espèces pour les Besoins de la Pêche, Vertébrés, Vol. 2, FAO, Rome, 976-980.
[32] Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W. (1997) Parasitology Meets Ecology on Its Own Terms: Margolis et al. Revisited. Journal of Parasitology, 83, 575-583.
[33] Zar, J.H. (1996) Biostatistical Analysis. 3rd Edition, Prentice-Hall, Upper Saddle River.
[34] Brodgar (2000) Software Package for Multivariate Analysis and Multivariate Time Series Analysis. Highland Statistics Ltd., Aberdeen.
[35] Dorman, J.A. (1991) Investigations onto the Biology of the Garfish, Belone belone (L.), in Swedish Waters. Journal of Fish Biology, 39, 59-69.
[36] Oliva, M.E., Valdivia, I.M., Costa, G., Freitas, N., Pinheiro de Carvalho, M.A., Sanchez, Z.L. and Luque, J.L. (2008) What Can Metazoan Parasites Reveal about the Taxonomy of Scomber japonicus Houttuyn in the Coast of South America and Madeira Islands. Journal of Fish Biology, 72, 545-554.
[37] Oliva, M.E. and Ballon, I. (2002) Metazoan Parasites of the Chilean Hake Merluccius gayi gayi as a Tool for Stock Discrimination. Fisheries Research, 56, 313-320.
[38] Poulin, R. (1995) “Adaptive” Changes in the Behaviour of Parasitized Animals: A Critical Review. International Journal for Parasitology, 25, 1371-1383.
[39] Sepúlveda, F., Marín, S. and Carvajal, J. (2004) Metazoan Parasites in Wild Fish and Farmed Salmon from Aquaculture Sites in Southern Chile. Aquaculture, 235, 89-100.
[40] Oliva, M.E., González, M. and Acuria, E. (2004) Metazoan Parasites Fauna as a Biological Tag for the Habitat of the Flounder Hippoglossina macrops from Northern Chile, in a Depth Gradient. Journal of Parasitology, 90, 1374-1377.
[41] González, M.T., Barrientos, C. and Moreno, C.A. (2006) Biogeographical Patterns in Endoparasitic Communities of a Marine Fish (Sebastes capensis Gmeli) with Extended Range in the Southern Hemisphere. Journal of Biogeography, 33, 1086-1095.
[42] González, M.T., Vásquez, R. and Acu?a, E. (2008) Biogeographic Patterns of Metazoan Parasites of the Bigeye Flounder Hippoglossina macrops in the Southeastern Pacific Coast. Journal of Parasitology, 94, 429-435.
[43] Henriquez, V.P., González, M.T., Licandeo, R. and Carvajal, J. (2011) Metazoan Parasite Communities of Rock Cod Eleginops maclovinus along Southern Chilean Coast and Their Use as Biological Tags at a Local Spatial Scale. Journal of Fish Biology, 79, 1851-1865.
[44] Sever, T.M., Bayhan, B., Bilge, G. and Taskavak, E. (2009) Diet Composition of Belone belone (Linnaeus, 1761) (Pisces: Belonidae) in the Aegean Sea. Journal of Applied Ichthyology, 25, 702-706.
[45] Zorica, B. and Cikes Kec, V. (2012) Prelminary Observations on Feeding Habits of Garfish Belone belone (L., 1761) in the Adriatic Sea. Croatian Journal of Fisheries, 70, 53-60.
[46] Machado, M.H., Pavanelli, G.C. and Takemoto, R.M. (1996) Structure and Diversity of Endoparasitic Infracommunities and the Trophic Level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Memorias do Instituto Oswaldo Cruz, 91, 441-448.
[47] Muňoz, G. and Cribb, T.H. (2005) Parasite Communities and Diet of Coris batuensis (Pisces: Labridae) from Lizard Island, Great Barrier Reef. Memoirs of the Queensland Museum, 52, 191-198.
[48] Katsanevakis, S., Lefkaditou, E., Galinou-Mitsoudi, S., Koutsoubas, D. and Zenetos, A. (2008) Molluscan Species of Minor Commercial Interest in Hellenic Seas: Distribution, Exploitation and Conservation Status. Mediterranean Marine Science, 9, 77-118.
[49] Ben mustapha, K. and Afli, A. (2007) Quelques traits de la biodiversité marine de Tunisie. Proposition d’aires de conservation et de gestion. In: Report of the MedSudMed Expert Consultation on Marine Protected Areas and Fisheries Management. MedSudMed Technical Documents, N° 3, GCP/RER/010/ITA/MSM-TD-03, 32-55.
[50] Brandhorst, W. (1977) Les conditions du milieu au large des c?tes tunisiennes. Bulletin National d’Océanographie et de Pêche Salammb?, 4, 129-220.
[51] Ben othman, S. (1973) Le sud tunisien (golfe de Gabès), hydrologie, sédimentologie, flore et faune. Thèse de 3ème cycle, Faculté des Sciences de Tunis, 166 p.
[52] Guillaumont, B., Ben mustapha, S., Ben moussa, H., Zaouali, J., Soussi, N., Ben mammou, A. and Cariou, C. (1995) Pollution Impact Study in Gabès Gulf (Tunisia) Using Remote Sensing Data. The Marine Technology Society, 29, 46-58.
[53] Klimpel, S. and Palm, H.W. (2011) Anisakid Nematode (Ascaridoidea) Life Cycles and Distribution: Increasing Zoonotic Potential in the Time of Climate Change? In: Mehlhorn, H., Ed., Progress in Parasitology, Parasitology Research Monographs, Springer, Berlin Heidelberg, 2, 201-222.
[54] Widmann, M. (2013) Impact of Large-Scale Environmental Features Changes on Host-Parasite Interaction in Marine and Freshwater Ecosystems. BioSciences Master Reviews, 1-9.
[55] Poulin, R. and Morand, S. (1999) Geographical Distances and the Similarity among Parasite Communities of Conspecific Host Populations. Parasitology, 119, 369-374.
[56] Poulin, R. (2003) The Decay of Similarity with Geographical Distance in Parasite Communities of Vertebrate Hosts. Journal of Biogeography, 30, 1609-1615.
[57] MacKenzie, K. (1987) Parasites as Indicators of Host Populations. International Journal for Parasitology, 17, 345-352.

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