Population dynamics of two diplectanid species (Monogenea) parasitising sparid hosts (Sparidae)

Abstract

Economically important sparid fish species, gilthead (Sparus aurata) and white seabream (Diplodus sargus) (Sparidae) are frequently parasitised by diplectanid monogeneans, known to induce severe losses in farming conditions. We have analysed population dynamic of two diplectanid species, Lamellodiscus echeneis and Lamellodiscus ignoratus (Monogenea: Diplectanidae) collected from two bream species in the Beymelek Lagoon (southwest coast of Turkey), comparing it between different host variables (fish size, age and sex) in order to have insight in parasites’ ecology, important for managing parasitosis in the intensive aquaculture system. In seabream (N = 127), L. echeneis prevalence was 46.5 % (exact 95 % confidence limits 38.90-54.14), mean abundance 5.64 (bootstrap 95 % confidence limits 4.20–7.65) and mean intensity 12.14 (bootstrap 95 % confidence limits 9.49–15.59). In white seabream (N = 102), L. ignoratus prevalence was 24.5 % (exact 95 % confidence limits 16.53–34.03), mean abundance 1.73 (bootstrap 95 % confidence limits 0.98–3.21) and mean intensity 7.04 (bootstrap 95 % confidence limits 4.60–11.40). Parasites’ parameters differed only between seasons in both hosts and between age categories in gilthead, but not in white seabream.

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References

  1. Akmirza A (2010) Investigation of the monogenean trematods and crustecean parasites of the cultured and wild marine fishes near Salih Island. Kafkas Univ Vet Fak Derg 16:S353–S360, In Turkish, with English abstract

    Google Scholar 

  2. Amine F, Euzet L, Kechemir-Issad N (2006) Description de deux nouvelles especes de Lamellodiscus Johnston & Tiegs, 1922 (Monogenea: Diplectanidae) du groupe morphologique ‘ignoratus’, parasites de Diplodus sargus et D. vulgaris (Teleostei: Sparidae). Syst Parasitol 64:37–45

    Article  PubMed  CAS  Google Scholar 

  3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust J Ecol 26:32–46

    Google Scholar 

  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, p 214

    Google Scholar 

  5. Antonelli L, Quilichini Y, Marchand B (2010) Biological study of Furnestinia echeneis Euzet and Audouin 1959 (Monogenea: Monopisthocotylea: Diplectanidae), parasite of cultured gilthead sea bream Sparus aurata (Linnaeus 1758) (Pisces: Teleostei) from Corsica. Aquaculture 307:179–186

    Article  Google Scholar 

  6. Aydogdu A, Kostadinova A, Fernandez M (2003) Variations in the distribution of parasites in the common carp, Cpyrinus carpio, from Lake Iznik, Turkey: population dynamics related to season and host size. Helminthologia 40:33–40

    Google Scholar 

  7. Bagenal TB, Tesch FW (1978) Age and growth. In: Bagenal TB (ed) Method for assessment of fish production in freshwater, 3rd edn. Blackwell, Oxford, pp 101–136

    Google Scholar 

  8. Bray RA (2001) Monogenea. In: Costello MJ, Emblow C, White RJ (eds) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Coll Patrim Natur 50:142–146

  9. Buchmann K, Lindenstrom T (2002) Interaction between monogenean parasites and their fish host. Int J Parasitol 32:309–319

    Article  PubMed  Google Scholar 

  10. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

  11. Cecchini S, Saroglia M, Berni P, Cognetti Varriale AM (1998) 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

    Article  Google Scholar 

  12. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth, p 192

    Google Scholar 

  13. Desdevises Y (2001) The phylogenetic position of Furnestinia echeneis (Monogenea, Diplectanidae) based on molecular data: a case of morphological adaptation? Int J Parasitol 31:205–208

    Article  PubMed  CAS  Google Scholar 

  14. Dogiel V (1970) Ecology of the parasites of freshwater fishes. In: Dogiel VA, Petrushevski GK, Polyanski YI (eds) Parasitology of fishes. TFH Publications, Hong Kong, pp 1–47

    Google Scholar 

  15. Euzet L, Combes C, Caro A (1993) A checklist of Monogenea of Mediterranean fish. Second international symposium on Monogenea. Montpellier–Sète, pp 5–8

  16. FAO (2011) Yerabook. Fisheries and aquaculture statistics. FAO, Rome, p 105

    Google Scholar 

  17. Fernando CH, Furtado JI, Gussev AV, Hanek G, Kakonge SA (1972) Methods for the study of freshwater fish parasites. Department of Biology, University of Waterloo, Waterloo, p 76

    Google Scholar 

  18. Fioravanti ML, Caffara M, Florio M, Gustinelli A, Marcer F, Quaglio F (2006) Parasitic diseases of marine fish: epidemiological and sanitary considerations. Parasitologia 48:15–18

    CAS  Google Scholar 

  19. Gussev AV (1983) Methods for collecting and processing fish parasitic monogenean material. Academi Nauk USSR, Leningrad, p 47, In Russian

    Google Scholar 

  20. Hanzelova V, Zitnan R (1985) Epizootiological importance of the concurrent monogenean invasion in the carp. Helminthologia 22:277–283

    Google Scholar 

  21. Ibarz A, Fernandez-Borras J, Blasco J, Gallardo MA, Sanchez J (2003) Oxygen consumption and feeding rates of gilthead sea bream (Sparus aurata) reveal lack of acclimation to cold. Fish Physiol Biochem 29:313–321

    Article  CAS  Google Scholar 

  22. Keser R, Bray RA, Oguz MC, Celen S, Erdogan S, Doguturk S, Aklanoglu G, Marti B (2007) Helminth parasites of digestive tract of some teleost fish caught in the Dardanelles at Canakkale, Turkey. Helminthologia 44:217–221

    Article  Google Scholar 

  23. Khalil AI (1981) Studies on some parasitic helminthes in some marine fish. MSc dissertation, Alexandria University

  24. Kir I (1998) Investigation of Parasites of carp (Cyprinus carpio L., 1758) and barbus (Barbus capito pectoralis L., 1758) living in Karacaören Dam Lake. Dissertation, Süleyman Demirel University Institute of Science

  25. Koskivaara M, Valtonen ET, Prost M (1991) Dactylogyrids on the gills of roach in central Finland: features of infection and species composition. Int J Parasitol 21:565–572

    Article  PubMed  CAS  Google Scholar 

  26. Koyun M, Altunel FN (2007) Metazoan Parasites of Bleak (Alburnus alburnus), Crucian Carp (Carassius carassius) and Golden Carp (Carassius auratus) in Enne Dam Lake, Turkey. Int J Zool Res 3:94–100

    Article  Google Scholar 

  27. Kutlu H, Özturk MO (2006) An investigation on anatomy, morphology and ecology of metazoan parasites of Cyprinus carpio Linnaeus, 1758 (common carp) from Lake Karamık (Afyonkarahisar). Ege Univ J Fish Aquat Sci 23:389–393

    Google Scholar 

  28. Lagler KF (1966) Freshwater fishery. Biology Publ, Dubuque, pp 62–74

    Google Scholar 

  29. Laiz-Carrion R, Sangiao-Alvarellos S, Guzman JM, Martin del Rio MP, Soengas JL, Mancera JM (2005) Growth performance of gilthead seabream Sparus aurata in different osmotic conditions: implications for osmoregulation and energy metabolism. Aquaculture 250:849–861

    Article  CAS  Google Scholar 

  30. Mercier L, Mouillot D, Bruguier O, Vigliola L, Darnaude AM (2012) Multi-element otolith fingerprints unravel sea—lagoon lifetime migrations of gilthead sea bream Sparus aurata. Mar Ecol Prog Ser 444:175–194

    Article  Google Scholar 

  31. Merella P, Cherchi S, Salati F, Garippa G (2005) Parasitological survey of sharpsnout seabream Diplodus puntazzo (Cetti, 1777) reared in sea cages in Sardinia (western Mediterranean). Bull Eur Assoc Fish Pathol 25:140–147

    Google Scholar 

  32. Meyer MC, Vik R (1968) Observation on Diphyllobothrium sebago—plerocercoids in the fish host. Proc Helminthol Soc Wash 35:92–96

    Google Scholar 

  33. Mladineo I (2004) Monogenean parasites in Adriatic cage-reared fish. Acta Adriat 45:65–73

    Google Scholar 

  34. Mladineo I, Maršić Lučić J (2007) Host switch of Lamellodiscus elegans (Monogenea: Monopisthocotylea) and Sparicotyle chrysophrii (Monogenea: Polyopisthocotylea) between cage-reared sparids. Vet Res Commun 31:153–160

    Article  PubMed  CAS  Google Scholar 

  35. Mladineo I, Petrić M, Šegvić T, Dobričić N (2010) Scarcity of parasite assemblages in the Adriatic-reared European sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata). Vet Parasitol 174:131–138

    Article  PubMed  Google Scholar 

  36. Mladineo I, Šegvić Bubić T, Stanić R, Desdevises Y (2013) Morphological plasticity and phylogeny in a monogenean parasite transferring between wild and reared fish populations. PLoS ONE 8(4):e62011. doi:10.1371/journal.pone.0062011

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  37. Nie P, Kennedy CR (1991) Occurrence and seasonal dynamics of Pseudodactylogyrus anguilla (Yin and Sproston) (Monogenea) in eel, Anguilla anguilla (L), in England. J Fish Biol 39:897–900

  38. Oliver G (1969) Recherches sur les Diplectanidae (Monogenea) parasites de Téléostéens du Golfe du Lion. II. Lamellodiscinae nov. sub. fam. Vie Mil 20:43–72

  39. Oliver G (1982) Microcotyle chrysophrii Van Beneden et Hesse, 1863 (Monogenea, Polyopisthocotylea, Microcotylidae) parasite de Sparus aurata Linnaeus, 1758 (Teleostei, Sparidae) dans les etangs littoraux du Languedoc – Roussillon (France). Parasitologia 20:113–118, In French

    Google Scholar 

  40. Özan T, Kır I, Barlas M (2008) Helminth parasites of common carp (Cpyrinus carpio L., 1758) in Beysehir Lake and populations dynamics related to month and host size. Turk J Fish Aquat Sci 8:201–205

    Google Scholar 

  41. Ozer A (2002) Co-existence of Dactylogyrus anchoratus Dujardin, 1845 and D. extensus Muller & Van Cleave, 1932 (Monogenea), parasites of common carp (Cprinus carpio). Helminthologia 39:45–50

    Google Scholar 

  42. Özer A, Erdem O (1999) The relationship between occurrence of ectoparasites temperature and culture conditions a comparison of farmed and wild common carp (Cyprinus carpio L.) in the Sinop Region of Northern Turkey. J Nat Hist 33:483–491

    Article  Google Scholar 

  43. Özer A, Özturk T (2004) Prevalence and Intensity of Gyrodactylus arcuatus Bychowsky, 1933 (Monogenea) infestations on the three-spined stickleback, Gasterosteus aculeatus L., 1758. Turk J Vet Anim Sci 28:807–812

    Google Scholar 

  44. Özturk MO (2002) Metazoan parasites of the tench (Tinca tinca L.) from Lake Uluabat. Is J Zool 48:285–293

    Article  Google Scholar 

  45. Özturk MO, Altunel FN (2006) Occurrence of Dactylogyrus infection linked to seasonal changes and host fish size on four cyprinid fishes in lake Manyas, Turkey. Acta Zool Acad Sci Hung 52:407–415

    Google Scholar 

  46. Paperna I, Colorni A, Gordin H, Kissil GW (1977) Diseases of Sparus aurata in marine culture at Elat. Aquaculture 10:195–213

    Article  Google Scholar 

  47. Pickering AD, Christie P (1980) Sexual differences in the incidence and severity of ectoparasitic infestation of brown trout, Salmo trutta L. J Fish Biol 16:669–683

    Article  Google Scholar 

  48. Poisot T, Desdevises Y (2010) Putative speciation events in Lamellodiscus (Monogenea: Diplectanidae) assessed by a morphometric approach. Biol J Linn Soc 99:559–569

    Article  Google Scholar 

  49. Poisot T, Verneau O, Desdevises Y (2011) Morphological and molecular evolution are not linked in Lamellodiscus (Plathyhelminthes, Monogenea). PLoS ONE 6, E26252

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  50. Pojmanska T (1994) Infection of common carp, and three introduced herbivorous fish from Zabieniec fish farm, in relation to their sizes. Acta Parasitol 86:228–232

    Google Scholar 

  51. Radujković BM, Euzet L (1989) Faune des parasites de poissons marins des côtes du Monténégro (Adriatique Sud). Acta Adriat 30:51–135, In French

    Google Scholar 

  52. Reiczigel J, Rózsa L (2005) Quantitative Parasitology 3.0. Budapest

  53. Reversat J, Silan P, Maillard C (1992) Structure of monogenean populations, ectoparasites of the gilthead sea bream Sparus aurata. Mar Biol 112:43–47

    Article  Google Scholar 

  54. Silan P, Cabral P, Maillard C (1985) Enlargement of the host rang of Polylabris tubicirrus (Monogenea, Polyopisthocotylea) under fish-farming conditions. Aquaculture 45:267–270

    Article  Google Scholar 

  55. Šimková A, Jarkovský J, Koubková B, Baruš V, Prokeš M (2005) Associations between fish reproductive cycle and the dynamic of metazoan parasite infections. Parasitol Res 95:65–72. doi:10.1007/s00436-004-1261-y

    Article  PubMed  Google Scholar 

  56. Sitjà-Bobadilla A, Alvarez-Pellitero P (2009) Experimental transmission of Sparicotyle chrysophrii (Monogenea: Polyopisthocotylea) to gilthead seabream (Sparus aurata) and histopathology of infection. Folia Parasitol 56:143–151

    Article  PubMed  Google Scholar 

  57. Sönmez S (1996) Investigation of parasitic fauna of fishes in Mogan Lake. MSc dissertation, Ankara University Institute of Science

  58. Toksen E (2006) Occurrence of gill parasite Lamellodiscus ignoratus (Palombi, 1943) (Monogenea: Diplectanidae) in cultured sharp-snout sea bream, Diplodus puntazzo (Cetti, 1777) from Izmir, Turkey. Bull Eur Assoc Fish Pathol 26:174–179

    Google Scholar 

  59. Tort L, Rotllant J, Liarte C, Acerete L, Hernandez A, Ceulemans S, Coutteau P, Padros F (2004) Effects of temperature decrease on feeding rates, immune indicators and histopathological changes of gilthead sea bream Sparus aurata fed with an experimental diet. Aquaculture 229:55–65

    Article  Google Scholar 

  60. Yagci MA (2006) The macrobenthic algae of Beymelek Lagoon (Antalya-Turkey). Turk J Fish Aquat Sci 6:137–147

    Google Scholar 

  61. Yamaguti S (1985) Systema Helminthum Monogenea and Apisdocotylea, Vol. IV. Wiley, New York, p 699

    Google Scholar 

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Ethical statement

Fish sampling complies with current laws in Turkey (Official Gazette of the Republic of Turkey, February 15, 2014, No. 28914: Regulation of working methods and principles of ethical committees for animal experiments, T.C. Ministry of Forestry and Water Affairs).

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Correspondence to Ivona Mladineo.

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Emre, Y., Emre, N., Aydogdu, A. et al. Population dynamics of two diplectanid species (Monogenea) parasitising sparid hosts (Sparidae). Parasitol Res 114, 1079–1086 (2015). https://doi.org/10.1007/s00436-014-4278-x

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Keywords

  • Sparus aurata
  • Diplodus sargus
  • Lamellodiscus echeneis
  • Lamellodiscus ignoratus
  • Diplectanidae
  • Population dynamic