Parasitology Research

, Volume 110, Issue 3, pp 1147–1157 | Cite as

Parasite communities and feeding ecology of the European sprat (Sprattus sprattus L.) over its range of distribution

Original Paper

Abstract

The metazoan parasite fauna and feeding ecology of 165 Sprattus sprattus (L., 1758) was studied from different geographic regions (Baltic Sea, North Sea, English Channel, Bay of Biscay, Mediterranean Sea). A total of 13 metazoan parasite species were identified including six Digenea, one Monogenea, two Cestoda, two Nematoda and two Crustacea. Didymozoidae indet., Lecithocladium excisum and Bomolochidae indet. represent new host records. The parasite species richness differed according to regions and ranged between 3 and 10. The most species-rich parasite fauna was recorded for sprats from the Bay of Biscay (North Atlantic), and the fishes from the Baltic Sea contained the lowest number of parasite species. More closely connected geographical regions, the North Sea, English Channel and Bay of Biscay, showed more similar parasite component communities compared with more distant regions. From the examined stomachs of S. sprattus, a total of 11 different prey items were identified, including Mollusca, Annelida, Crustacea and Tunicata. The highest number of prey organisms belonged to the crustaceans. The variety of prey items in the stomach was reflected by the parasite community differences and parasite species richness from the different regions. The feeding ecology of the fish at the sampled localities was responsible for the observed parasite composition and, secondarily, the zoogeographical distribution of the parasites, questioning the use of the recorded sprat parasites as biological indicators for environmental conditions and change.

References

  1. Abollo E, D’Amelio S, Pascual S (2001a) Fitness of the marine parasitic nematode Anisakis simplex s. str. in temperate waters of the NE Atlantic. Dis Aquat Organ 45:131–139PubMedCrossRefGoogle Scholar
  2. Abollo E, Gestal C, Pascual S (2001b) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87(6):492–499PubMedCrossRefGoogle Scholar
  3. Arthur JR (1997) Recent advances in the use of parasites as biological tags for marine fish. In: Flegel TW, MacRae IH (eds) Diseases in Asian aquaculture III. Fish Health Section, Asian Fisheries Society, Manila, pp 141–154Google Scholar
  4. Arthur JR, Albert E (1993) Use of parasites for separating stocks of Greenland halibut (Reinhardtius hippoglossoides) in the Canadian Northwest Atlantic. Can J Fish Aquat Sci 50(10):2175–2181CrossRefGoogle Scholar
  5. Bell JJ, Barnes KA (2003) Effect of disturbance on assemblages: an example using Porifera. Biol Bull 205:144–159PubMedCrossRefGoogle Scholar
  6. Berland B (1998) Biology of Hysterothylacium species. In: Tada I, Kojima S, Tsuji M (eds) Proceedings of the 9th International Congress on Parasitology, Chiba, Japan, pp 373–378Google Scholar
  7. Bush O, Lafferty AD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on his own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedCrossRefGoogle Scholar
  8. Cardinale M, Casini M, Arrhenius F (2002) The influence of biotic and abiotic factors on the growth of sprat (Sprattus sprattus) in the Baltic Sea. Aquat Living Res 15:272–281CrossRefGoogle Scholar
  9. Cardinale M, Casini M, Arrhenius F, Håkansson N (2003) Diel spatial distribution and feeding activity of herring (Clupea harengus) and sprat (Sprattus sprattus) in the Baltic Sea. Aquat Living Res 16:283–292CrossRefGoogle Scholar
  10. Casini M, Cardinale M, Hjelm J (2006) Inter-annual variation in herring, Clupea harengus, and sprat, Sprattus sprattus, condition in the central Baltic Sea: what gives the tune? Oikos 112:638–650CrossRefGoogle Scholar
  11. Dailianis T, Limborg M, Hanel R, Bekkevold D, Lagnel J, Magoulas A, Tsigenopoulos CS (2008) Characterization of nine polymorphic microsatellite markers in spratt (Sprattus sprattus L.). Mol Ecol Resour 8:861–863PubMedCrossRefGoogle Scholar
  12. Dimitrov GI, Bray RA, Gibson DI (1999) A rediscription of Pseudobacciger harengulae (Yamagutti, 1938) (Digenea: Faustulidae) from Sprattus sprattus phalericus (Risso) and Engraulis encrassicholus ponticus Alexandrov off the Bulgarian Black Sea coast, with a review of the genus Pseudobacciger Nahhas & Cable, 1964. Syst Parasitol 43:133–146PubMedCrossRefGoogle Scholar
  13. Dzikowski R, Paperna I, Diamant A (2003) Use of fish parasite species richness indices in analyzing anthropogenically impacted coastal marine ecosystems. Helgol Mar Res 57:220–227CrossRefGoogle Scholar
  14. Fiedler K (1991) Fische: In: Kaestner A. (eds) Lehrbuch der speziellen Zoologie. 2. Teil, Bd. II. Gustav Fischer Verlag Stuttgart: pp 498Google Scholar
  15. Fischer E (1955) Die parasitischen Würmer der wirtschaftlich wichtigsten Ostseefische. PhD thesis, Humboldt-University Berlin: 136 SeitenGoogle Scholar
  16. Gibson DI, Bray RA (1986) The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bulletin of the British Museum (Natural History), Zoology Series 51:1–125Google Scholar
  17. Gibson DI, Harris EA, Bray RA, Jepson PD, Kuiken T, Baker JR, Simpson VR (1998) A survey of the helminth parasites of cetaceans stranded on the coast of England and Wales during the period 1990–1994. J Zool London 244:563–574CrossRefGoogle Scholar
  18. Groenewold S (1992) Zur Bedeutung von Kleinfischparasiten im Nordfriesischen Wattenmeer. MSc thesis, Universität Hamburg: 86 SeitenGoogle Scholar
  19. Groenewold S, Berghahn R, Zander CD (1996) Parasite communities of four fish species in the Wadden Sea and the role of fish discarded by the shrimp fisheries in parasite transmission. Helgoländer Meeresuntersuchungen 50:69–85CrossRefGoogle Scholar
  20. Herreras MV, Kaarstad SE, Balbuena JA, Kinze CC, Raga JA (1997) Helminth parasites of digestive tract of the harbour porpoise Phocoena phocoena in Danish waters: a comparative geographical analysis. Dis Aquat Organ 28:163–167CrossRefGoogle Scholar
  21. Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  22. Kelly-Gerreyn BA, Hydes DJ, Jégou AM, Lazure P, Fernand LJ, Puillat I, Garcia-Soto C (2006) Low salinity intrusions in the western English Channel. Continent Shelf Res 26(11):1241–1257CrossRefGoogle Scholar
  23. Kleinertz S (2010) Fish parasites as bioindicators: environmental status of coastal marine ecosystems and a grouper mariculture farm in Indonesia. PhD thesis of Natural Sciences, Department 2 (Biology/Chemistry), University of Bremen, 263 ppGoogle Scholar
  24. Klimpel S, Palm HW (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, vol 2. Springer, Berlin. doi:10.1007/978-3-642-21396-0_11
  25. Klimpel S, Rückert S (2005) Life cycle strategy of Hysterothylatium aduncum to become the most abundant anisakid fish nematode in the North Sea. Parasitol Res 97:141–149PubMedCrossRefGoogle Scholar
  26. Klimpel S, Palm HW, Seehagen A (2003) Metazoan parasites and feeding behaviour of four small-sized fish species from the central North Sea. Parasitol Res 91:290–297PubMedCrossRefGoogle Scholar
  27. Klimpel S, Palm HW, Rückert S (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9PubMedCrossRefGoogle Scholar
  28. Klimpel S, Kleinertz S, Hanel R, Rückert S (2007) Genetic variability in Hysterothylacium, a raphidascarid nematode isolated from sprat (Sprattus sprattus) of different geographical areas of the northeastern Atlantic. Parasitol Res 101:1425–1430PubMedCrossRefGoogle Scholar
  29. Klimpel S, Kleinertz S, Palm HW (2008) Distribution of parasites from red mullets (Mullus surmuletus L., Mullidae) in the North Sea and Mediterranean Sea. Bull Fish Biol 10:25–38Google Scholar
  30. Klimpel S, Busch MW, Kellermanns E, Kleinertz S, Palm HW (2009) Metazoan deep-sea fish parasites. Acta Biologica Benrodis, Supplement 11, Natur & Wissen Verlag, Solingen: 384 SeitenGoogle Scholar
  31. Køie M (1979) On the morphology and life-history of Derogenes varicus (Müller, 1784) Looss, 1901 (Trematoda, Hemiuridae). Zeitschrift für Parasitenkunde (Parasitol Res) 59:67–78CrossRefGoogle Scholar
  32. Køie M (1990) On the morphology and life-history of Hemiurus luehei Odhner, 1905 (Digenea: Hemiuridae). J Helminthol 64:193–202PubMedCrossRefGoogle Scholar
  33. Køie M (1992) Life cycle and structure of the fish digenean Brachyphallus crenatus (Hemiuridae). J Parasitol 78:338–343PubMedCrossRefGoogle Scholar
  34. Køie M (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (nematoda, Ascaridoidea, Anisakidea). Can J Zool 71:1289–1296CrossRefGoogle Scholar
  35. Køie M, Lester RJG (1985) Larval didymozoids (Trematoda) in fishes from Moreton Bay, Australia. Proc Helminthol Soc Wash 52:196–203Google Scholar
  36. Lazure P, Jégou AM, Kerdreux M (2006) Analysis of salinity measurements near islands on the French continental shelf of the Bay of Biscay. In: Morán XAG, Rodriguez JM, Petigas P (eds) Oceanography of the Bay of Biscay. Scientia Marina, 70S1, Barcelona (Spain), pp 7–14. ISSN: 0214–8358Google Scholar
  37. Limborg MT, Pedersen JS, Hemmer-Hansen J, Tomkiewicz J, Bekkevold D (2009) Genetic population structure of European sprat Sprattus sprattus: differentiation across a steep environmental gradient in a small pelagic fish. Marine Ecol Progr Ser 379:213–224CrossRefGoogle Scholar
  38. Love MS, Moser M (1983) A checklist of parasites of Californian, Oregon and Washington marine and estuarine fishes. NOAA Technical Report NMFS SSRF 777:1–577Google Scholar
  39. MacKenzie K (1983) Parasites as biological tags in fish population studies. Adv Appl Biol 7:251–331Google Scholar
  40. MacKenzie K (1985) The use of parasites as biological tags in population studies of herring (Clupea harengus L.) in the North Sea and to north and west of Scotland. J Intl Council Explor Sea 42:33–64Google Scholar
  41. MacKenzie K (1987) Long-term changes in the prevalence of two helminth parasites (Cestoda: Trypanorhyncha) infecting marine fish. J Fish Biol 31:83–87CrossRefGoogle Scholar
  42. MacKenzie K (1990) Cestode parasites as biological tags for mackerel (Scomber scombrus L.) in the northeast Atlantic. J Intl Council Explor Sea 46:155–166Google Scholar
  43. Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, LondonGoogle Scholar
  44. Marcogliese DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Rev Fish Biol Fisheries 5:336–371CrossRefGoogle Scholar
  45. Marcogliese DJ (1996) Larval parasitic nematodes infecting marine crustaceans in eastern Canada. 3. Hysterothylacium aduncum. J Helminthol Soc Washington 63(1):12–18Google Scholar
  46. Marcogliese DJ (2002) Food webs and the transmission of parasites to marine fish. Parasitology 124:83–99CrossRefGoogle Scholar
  47. Margolis L, Arthur JR (1979) Synopsis of the parasites of fishes of Canada. Bull Fisheries Res Board Canada 199:1–269Google Scholar
  48. Möllmann C, Kornilovs G, Fetter M, Köster FW (2004) Feeding ecology of central Baltic Sea herring and sprat. J Fish Biol 65:1563–1581CrossRefGoogle Scholar
  49. Nikolaeva VM (1965) On the developmental cycle of trematodes belonging to the family Didymozoidae. Zlogicheski Zhurnal 44:1317–1327Google Scholar
  50. Palm HW (2011) Fish parasites as biological indicators in a changing world: can we monitor environmental impact and climate change? In: Mehlhorn H (ed) Progress in parasitology. Parasitology Research Monographs, vol 2, Springer, Berlin. doi:10.1007/978-3-642-21396-0_12
  51. Palm HW, Dobberstein RC (1999) Occurrence of trichodinid ciliates (Peritricha: Urceolariidae) in the Kiel Fjord, Baltic Sea, and its possible use as a biological indicator. Parasitol Res 85:726–732PubMedCrossRefGoogle Scholar
  52. Palm HW, Rückert S (2009) A new approach to visualize fish and ecosystem health by using parasites. Parasitol Res 105:539–553PubMedCrossRefGoogle Scholar
  53. Palm HW, Klimpel S, Bucher C (1999) Checklist of metazoan fish parasites of German coastal waters. Berichte aus dem Institut für Meereskunde 307:1–148Google Scholar
  54. Palm HW, Kleinertz S, Rückert S (2011) Parasite diversity as an indicator of environmental change?—An example from tropical grouper (Epinephelus fuscoguttatus) mariculture in Indonesia. Parasitology 138:1–11. doi:10.1017/S0031182011000011 CrossRefGoogle Scholar
  55. Pinkas L, Oliphant MD, Iverson ILK (1971) Food habits of albacore, bluefin tuna and bonito in Californian waters. California Fish and Game 152:1–105Google Scholar
  56. Reimer LW (1978) Parasiten von Sprotten III. Wissenschaftliche Konferenz zu Fragen der Physiologie und Biologie von Nutzfischen, 7.-8.9.1978 in Rostock, pp 147–152Google Scholar
  57. Rheinheimer G (ed) (1995) Meereskunde der Ostsee. 2. Auflage, Springer, 338 ppGoogle Scholar
  58. Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 239–301Google Scholar
  59. Rother K (1993) Der Mittelmeerraum. Teubner Studienbücher der Geographie,183 ppGoogle Scholar
  60. Sasal P, Mouillot D, Fichez R, Chifflet S, Kulbicki M (2007) The use of fish parasites as biological indicators of anthropogenic influences in coral-reef lagoons: a case study of Apogonidae parasites in New-Caledonia. Mar Pollut Bull 54:1697–1706PubMedCrossRefGoogle Scholar
  61. Strømnes E, Andersen K (2000) “Spring rise” of whaleworm (Anisakis simplex; Nematoda, Ascaridoidea) third stage larvae in some fish species from Norwegian waters. Parasitol Res 86:619–624PubMedCrossRefGoogle Scholar
  62. Sures B (2008) Host–parasite interactions in polluted environments. J Fish Biol 73:2133–2142CrossRefGoogle Scholar
  63. Tolonen A, Karlsbakk E (2003) The parasite fauna of the Norwegian spring spawning herring (Clupea harengus L.). ICES Journal of Marine Science 60:77–84CrossRefGoogle Scholar
  64. Vidal-Martínez VM, Pech D, Sures B, Purucker ST, Poulin R (2010) Can parasites really reveal environmental impact? Trends Parasitol 26(1):44–51PubMedCrossRefGoogle Scholar
  65. Williams HH, MacKenzie K, McCarthy AM (1992) Parasites as biological indicators of the population biology, migrations, diet and phylogenetics of fish. Rev Fish Biol Fisheries 2:144–176CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sonja Kleinertz
    • 1
    • 2
  • Sven Klimpel
    • 3
  • Harry W. Palm
    • 1
  1. 1.Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental SciencesUniversity of RostockRostockGermany
  2. 2.Leibniz Center for Tropical Marine Ecology GmbHBremenGermany
  3. 3.Biodiversity and Climate Research Centre (BiK-F)Goethe-University, Institute for Ecology, Evolution and DiversityFrankfurt am MainGermany

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