Abstract
The parasites of 536 European sea bass, Dicentrarchus labrax, were studied between January 2012 and December 2013 in six Corsican fish farms. The indicator value (IndVal) method, which combines measures of fidelity and specificity, has been used in this study. Because of its resilience to changes in abundance, IndVal is a particularly effective tool for ecological bioindicator. The IndVal method showed how season can influence the occurrence of parasite species in cultured sea bass and also identified parasites as bioindicators relative to fish farm location. The combination of specificity and fidelity highlighted several parasite species as significant indicators. A randomization test identified five parasite species as having a significant indicator value for season (the monogenean Diplectanum aequans; the copepods Lernanthropus kroyeri and Caligus minimus; the isopod Ceratothoa oestroides, and the myxosporidian Ceratomyxa labracis). If gills parasites are compared, they can be seen to be indicator species for two different seasons. The only Monogenea species D. aequans had fidelity and specificity more pronounced in winter, whereas both copepod species and the Isopoda revealed highest rates of infestation corresponding with an increase of water temperature. Four species have a significant indicator value for site location (D. aequans, L. kroyeri, C. minimus, and C. oestroides). The fact that the farm 6 was isolated on the east coast of Corsica may not have allowed the parasite to infect other farms. The presence of copepods on a single farm can also be explained according to salinity variations. Data for species composition and infection levels should help to improve the monitoring and management of parasitism in cultured sea bass populations.
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Abdel-Ghaffar F, Abdel-Gaber R, Abdel-Rahman B, Morsy K, Al Quraishy S, Saleh R, Mehlhorn H (2015) Molecular characterization and new geographical record of Lecithochirium priacanthi (Digenea: Hemiuridae) infecting the moontail bullseye fish Priacanthus hamrur (Perciformes: Priacanthidae) from the Red Sea, Egypt. Parasitol Res: In press. DOI 10.1007/s00436-4690x
Alvarez-Pellitero P, Sitjà-Bobadilla A (1993) Light and electron microscopical description of Ceratomyxa labracis n. sp. and a redescription of C. diplodae (Myxosporea: Bivalvulida) from wild and cultured Mediterranean sea bass Dicentrarchus labrax (L.) (Teleostei: Serranidae). Syst Parasitol 26:215–223
Aminot A, Kerouel R (2004) Hydologie des écosytèmes marins: paramètres et analyses. Collection Méthodes d’analyse en milieu marin, IFREMER
Antonelli L (2010) Impact du parasitisme sur la pisciculture en Corse. Suivi des parasitoses et étude des transferts de parasites depuis la faune sauvage vers les poissons élevés en mer ouverte. Thèse, Université de Corse, Pasquale Paoli
Antonelli L, Quilichini Y, Marchand B (2010) Sparicotyle chrysophrii (Van Beneden and Hesse 1863) (Monogenea: Polyopisthocotylea) parasite of cultured Gilthead sea bream Sparus aurata (Linnaeus 1758) (Pisces: Teleostei) from Corsica: ecological and morphological study. Parasitol Res 107:389–398
Antonelli L, Marchand B (2012) Metazoan parasites of the European sea bass Dicentrarchus labrax (Linnaeus 1758) (Pisces: Teleostei) from Corsica. In: Health and Environment in Aquaculture. Edited by Edmir Daniel Carvalho, Gianmarco Silva David and Reinaldo J. Silva, InTech, pp 43-62
Antonelli L, Quilichini Y, Marchand B (2012) Lernanthropus kroyeri (Van Beneden and Hesse 1851) parasitic Copepoda (Siphonostomatoidae, Lernanthropidae) of European cultured sea bass Dicentrarchus labrax (Linnaeus 1758) from Corsica: ecological and morphological study. Parasitol Res 110:959–1968
Ashley PJ (2006) Fish welfare: current issues in aquaculture. Appl Anim Behav Sci 104:199–235
Bahri L, Ben Hamida J, Ben Hassine OK (2002) Use of parasitic copepod, Lernanthropus kroyeri (Van Beneden, 1851) (Lernanthropidae) as a bio-indicator of two fish populations, Dicentrarchus labrax Linnaeus (1758) and Diplodus punctatus (Bloch, 1792) (Moronidae) in Tunisian inshore areas. Crustaceana 75:253–267
Bragoni G, Romestand B, Trilles JP (1984) Parasitoses à Cymothoidiens chez le loup Dicentrarchus labrax Linnaeus (1758) en élevage. 1. Ecologie parasitaire dans le cas de l’étang de Diana (Haute-Corse) (Isopoda, Cymothoidae). Crustaceana 44:47–51
Cecchini S, Saroglia M, Berni P, Cognetti-Varriale AM (1994) Influence of temperature on the life cycle of Diplectanum aequans (Monogenea, Diplectanidae), parasitic on sea bass, Dicentrarchus labrax (L.). J Fish Dis 21:73–75
Combes C (1990) When is a parasite pathogen? Metazoan parasitic diseases: concluding remarks. Pathology in Marine Science. Academic Press Inc. Publisher, pp 331–340
Combes C (2001) Interactions durables. Ecologie et évolution du parasitisme, edn. Collection d'e´cologie, Masson, Paris
Daszak P, Cunningham AA, Hyatt AD (2000) Wildlife ecology—emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449
Detsis V, Diamantopoulos J, Kosmas C (2000) Collembolan assemblages in Lesvos, Greece. Effects of differences in vegetation and precipitation. Acta Oecol 21:149–159
Devreker D, Souissi S, Winkler G, Forget-Leray J, Leboulenger F (2009) Effects of salinity, temperature and individual varaiability on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study. J Exp Mar Biol Ecol 368:113–123
Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
El-Madhi Y, Belghyti D (2006) Distribution de deux monogènes dans les individus hôtes de Trachinotus ovatus (L, 1758) de la côte de Mehdia. Biologie et Santé 6:65–76
El-Naggar MM (1994) Ecological studies on the monogenean parasites of the teleost Clarias lazera inhabiting Nile Delta Waters. M.Sc. Thesis. Zoology Department, Faculty of Sciences, Mansoura University, Egypt
F.A.O (2014) Food and Agriculture Organization of the United Nations: state of world fisheries and aquaculture Opportunities and challenges. Rome
Fernandez-Jover D, Faliex E, Sanchez-Jerez P, Sasal P, Bayle-Sempere JT (2010) Coastal fish farming does not affect the total parasite communities of wild fish in SW Mediterranean. Aquaculture 300:10–16
Fioravanti ML, Caffara M, Florio D, Gustinelli A, Marcer F, Quaglio F (2006) Parasitic diseases of marine fish: epidemiological and sanitary considerations. Parassitologia 48:15–18
Foata J, Mouillot D, Culioli JL, Marchand B (2006) Influence of season and host age on wild boar parasites in Corsica using indicator species analysis. J Helminthol 80:41–45
Gannicott AM, Tinsley RC (1998) Larval survival characteristics and behavior of the gill monogenean Discocotyle sagittata. Parasitology 47:491–498
Ghittino C, Latini M, Agnetti F, Panzieri C, Lauro L, Ciapelloni R, Petracca A (2003) Emerging pathologies in aquaculture: effects on production and food safety. Vet Res Commun 27:471–479
Gonzalez-Lanza C, Alvarez-Pellitero P, Sitjà-Bobadilla A (1991) Diplectanidae (Monogenea) infestations on sea bass, Dicentrarchus labrax (L.), from the Spanish area. Histopathology and population dynamics under culture conditions. Parasitol Res 77:307–314
H.L.P.E (2014) Sustainable fisheries and aquaculture for food security and nutrition. A report by the High Level Panel of Experts on Food Security and Nutrition of the Committee on World Food Security, Rome 2014
Holmes JC (1987) The structure of Helminth communities. Int J Parasitol 17:203–208
Hufnagel L, Bakonyi G, Vasarhelyi T (1999) New approach for habitat characterization based on species lists of aquatic and semiaquatic bugs. Environ Monit Assesss 58:305–316
Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z (2004) A review of the Impact of parasitic Copepods on marine aquaculture. Zool Stud 43:229–243
Kim KH, Ahn KJ, Kim CS (2001) Seasonal abundances of Prosomicrocotyla gotoi (Monogenea) and Opecoleus sphaericus (Digenea) from greenlings Hexagrammos otakii in a southern coastal area in Korea. Aquaculture 192:147–153
Kent ML (2000) Marine netpen farming leads to infections with some unusual parasites. Int J Parasitol 30:321–326
Lambert A, Maillard C (1975) Répartition branchiale de deux Monogènes : Diplectanum aequans (Wagener, 1857) Diesing 1858 et Diplectanum laubieri Lambert et Maillard 1974 (Monogenea, Monopisthocotylea) parasites simultanés de Dicentrarchus labrax (Téléostéens). Ann Parasitol Hum Comp 50:691–699
Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam
McAllen RJ, Taylor AC, Davenport J (1998) Osmotic and body density response in the harpacticoid copepod Tigriopus brevicornis in supralittoral rock pools. J Mar Biol 78:1143–1154
McCune B, Mefford MJ (1999) PC-ORD. Multivariate analysis of ecological data, Version 4. MjM Software Design. Gleneden Beach, Oregon, USA
McGeoch MA, Chown SL (1998) Scaling up the value of bioindicators. Trends Ecol Evol 13:46–47
Manera M, Dezfuli BS (2003) Lernanthropus kroyeri infections in farmed sea bass Dicentrarchus labrax: pathological features. Dis Aquat Org 57:177–180
Merino G, Barange M, Blanchard JL, Harle J, Holmes R, Allen I, Allison EH, Badjeck MC, Dulvy NK, Holt J, Jennings S, Mullon C, Rodwell LD (2012) Can marine fisheries and aquaculture meet fish demand from a growing human population in a changing climate? Glob Environ Chang 22:795–806
Mikusinki G, Gromadzki M, Chuylarecki P (2001) Woodpeckers as indicators of forest bird diversity. Conserv Biol 15:208–217
Mouillot D, Culioli JM, Do Chi T (2002) Indicator species analysis as a test of non-random distribution of species in the context of marine protected areas. Environ Conserv 29:385–390
Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folkes C, Lubchenco J, Mooney H, Troells M (2000) Effects of aquaculture on world fish supplies. Nature 405:1017–1024
Nowak BF (2007) Parasitic diseases in marine cage culture. An example of experimental evolution of parasites? Int J Parasitol 37:581–588
Oliver G (1984) Microcotyle chrysophrii Van Beneden et Hesse, 1863 (Monogenea, Polyopisthocotylea, Microcotylidae) parasite de Sparus aurata Linneaus, 1758 (Teleostei, Sparidae) dans les étangs littoraux du Languedoc-Roussillon (France). Bull. Soc Zool Fr 109:113–118
Paperna I, Colorni A, Gordin H, Kissil GW (1977) Diseaes of Sparus aurata in marine culture at Elat. Aquaculture 10:195–213
Quilichini Y, Foata J, Mouillot D, Mattei J, Marchand B (2010) The influence of altitude, hydrographic network and season on brown trout parasites in Corsica using indicator species analysis. J Helminthol 84:13–19
Robertsen G, Olstad K, Plaisans L, Buchmann L, Bakke TA (2008) Gyrodactylus salaris (Monogenea, Gyrodactylidae) infections on resident Arctic charr (Salvelinus alpinus) in southern Norway. Environ Biol Fish 83:99–105
Silan P, Maillard C (1989) Biologie compare du développement et discrimination des Diplectanidae ectoparasites du Bar (Teleostei). Ann Sci Nat, Zool 10:31–45
Stork NE, Samxays MJ (1995) Inventorying and monitoring. In: Heywood VH, Watson RT (eds) Global Biodiversity Assessment. United Nations Environment Program. University Press, Cambridge, United Kingdom, pp 453–543
Winger AC, Kanck M, Kristoffersen R, Knudsen R (2008) Seasonal dynamics and persistence of Gyrodactylus salaris in two riverine anadromous Arctic charr populations. Environ Biol Fish 83:117–123
Zimmer KD, Hanson MA, Butler MG (2000) Factors influencing invertebrate communities in prairie wetlands: a multivariate approach. Can J Fish Aquat Sci 57:76–85
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We are grateful to Corsican fish farmers for providing us fish sampling.
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Antonelli, L., Foata, J., Quilichini, Y. et al. Influence of season and site location on European cultured sea bass parasites in Corsican fish farms using indicator species analysis (IndVal). Parasitol Res 115, 561–568 (2016). https://doi.org/10.1007/s00436-015-4772-9
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DOI: https://doi.org/10.1007/s00436-015-4772-9