Distribution of ascaridoid nematodes (Nematoda: Chromadorea: Ascaridoidea) in fish from the Barents Sea

Authors

  • Katarzyna Najda University of Gdansk
  • Agnieszka Kijewska Laboratory of Genetics of Marine Organisms, Institute of Oceanology PAS, Sopot
  • Tomasz Kijewski Laboratory of Genetics of Marine Organisms, Institute of Oceanology PAS, Sopot
  • Kęstas Plauška Fisheries Service under the Ministry of Agriculture Division of Fisheries Research & Science, Lithuania
  • Jerzy Rokicki University of Gdansk

Keywords:

Ascaridoidea, Barents Sea, nematodes, parasites, Greenland halibut

Abstract

The Ascaridoidea are parasites with heteroxenous life cycles. The study shows that fish can be paratenic, intermediate, or final hosts for parasites, and parasitic fauna reflects the feeding behavior of the hosts. Each species of parasites has also different environmental preferences and host specificity. Parasitic nematodes of fish representing Pleuronectidae, Gadidae, Sebastidae, and Macrouridae were studied. Worms were collected separately from different infection sites: stomach, intestine, liver and body cavity. Nematodes were identified using both morphological and molecular methods (PCR-RFLP). Six nematode species were recorded: Anisakis simplex s.s., Contracaecum osculatum A, B, and C. osculatum C (s.s.), Hysterothylacium aduncum and Pseudoterranova bulbosa. Anisakis simplex s.s. was the most numerous nematode species of all catches combined. Differences in parasite species composition were related to the depth and location of sampling areas. In the fish from deep waters, the abundance of A. simplex s.s. decreased compared to fish from shallow waters and P. bulbosa was the dominant species. Ascaridoid species have specific preferences regarding the impact on various internal organs of fish, which is reflected in their abundance. The presence of Ascaridoidea in the Barents Sea is associated with the distribution of hosts and varying food preferences related to the age of fish. The abundance of parasites varied between different host species.

Downloads

Download data is not yet available.

References

Balbuena, J.A., Karlsbakk, E., Saksvik, M., Kvenseth, A.M. & Nylund, A. (1998). New data on the early development of Hysterothylacium aduncum (Nematoda, Anisakidae). Journal of Parasitology 84: 615–617. DOI: 10.2307/3284732.

Balbuena, J.A., Karlsbakk, E., Kvenseth, A.M., Saksvik, M. & Nylund, A. (2000). Growth and emigration of third-stage larvae of Hysterothylacium aduncum (Nematoda: Anisakidae) in larval herring Clupea harengus. Journal of Parasitology 86: 1271–1275. DOI: 10.1645/0022-3395(2000)086[1271:GAEOTS]2.0.CO;2.

Bowering, W.R. & Chumakov, A.K. (1989). Distribution and relative abundance of Greenland halibut (Reinhardtius hippoglossoides Walbaum) in the Canadian Northwest Atlantic from Davis Strait to the northern Grand Bank. Fisheries Research 7: 301–327. DOI: 10.1016/0165-7836(89)90064-7.

Bowering, W.R. & Lilly, G.R. (1992). Predation on shrimp (Pandalus borealis) by Greenland halibut (Reinhardtius hippoglossoides) and Atlantic Cod (Gadus morhua) off Labrador. ICES Council Meeting 1984/G: 54.

Brattey, J. & Davidson, W.S. (1996). Genetic variation within Pseudoterranova decipiens (Nematoda: Ascaridoidea) from Canadian Atlantic marine fishes and seals: Characterization by RFLP analysis of genomic DNA. Canadian Journal of Fisheries and Aquatic Sciences 53: 333–341. DOI: 10.1139/f95-196.

Brattey, J. & Stenson, G.B. (1993). Host specificity and abundance of parasitic nematodes (Ascaridoidea) from the stomachs of five phocid species from Newfoundland and Labrador. Canadian Journal of Zoology 71: 2156–2166. DOI: 10.1139/z93-303.

Bristow, G.A. & Berland, B. (1992). On the ecology and distribution of Pseudoterranova decipiens C (Nematoda: Anisakidae) in an intermediate host, Hippoglossoides platessoides, in northern Norwegian waters. International Journal of Parasitology 22: 203–208. DOI: 10.1016/0020-7519(92)90102-Q.

Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4): 575–583. DOI: 10.2307/3284227.

Chibani, M., Kijewska, A. & Rokicki, J. (2005). Sex and age of flounder Platichthysflesus (L.) and parasitic infection in the Gulf of Gdańsk. Oceanological and Hydrobiological Studies 34: 85–96.

Dalpadado, P. & Skjoldal, H.R. (1996). Abundance, maturity and growth of the krill species Thysanoessa inermis and T. longicaudata in the Barents Sea. Marine Ecology Progress Series 144: 175–183.

Dolgov, A.V., Yaragina, N.A., Ajiad, A.M., Mehl, S. & Bogstad, B. (1992). Daily rations of cod from the Barents Sea. PINROIMR Symposium 5; 1992.

Dwyer, K.S., Buren, A. & Koen-Alonso, M. (2010). Greenland halibut diet in the Northwest Atlantic from 1978 to 2003 as an indicator of ecosystem change. Journal of Sea Research 64: 436–445. DOI: 10.1016/j.seares.2010.04.006.

Dzido, J. (2011). Identyfikacja molekularna oraz zróżnicowanie wewnątrzgatunkowe pasożytniczych nicieni z rodziny Anisakidae. Unpublished doctoral dissertation. University of Gdańsk, Gdańsk, Poland, 133 p. (In Polish).

Fagerholm, H.P. (1991). Systematic implications of male caudal morphology in ascaridoid nematode parasites. Systematic Parasitology 19: 215–228. DOI: 10.1007/BF00011888.

Froese, R. & Pauly, D. (2017). FishBase. World Wide Web electronic publication. www.fishbase.org, version (06/2017).

Hoarau, G., Holla, S., Lescasse, R., Stam, W.T. & Olsen, J.L. (2002). Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus. Molecular Biology and Evolution 19: 2261–2264. DOI: 10.1093/oxfordjournals.molbev.a004049.

Hovde, S.C., Albert, O.T. & Nilssen, E.M. (2002). Spatial, seasonal and ontogenetic variation in diet of Northeast Arctic Greenland halibut (Reinhardtius hippoglossoides). ICES Journal of Marine Science 59: 421–437. DOI: 10.1006/jmsc.2002.1171.

Jørgensen, O.A. (1997). Pelagic occurrence of Greenland halibut, Reinhardtius hippoglossoides (Walbaum), in West Greenland waters. Journal of Northwest Atlantic Fishery Science 21: 39–50. DOI: 10.2960/J.v21.a3.

Karpiej, K., Dzido, J., Rokicki, J. & Kijewska, A. (2013). Anisakid nematodes of Greenland halibut Reinhardtius hippoglossoides from the Barents Sea. Journal of Parasitology 99(4): 650–654. DOI: 10.1645/GE-2987.1.

Kijewska, A., Rokicki, J., Sitko, J. & Wegrzyn, G. (2002). Ascaridoidea: a simple DNA assay for identification of 11 species infecting marine and freshwater fish, mammals, and fish-eating birds. Experimental Parasitology 101: 35–39. DOI: 10.1016/S0014-4894(02)00031-0.

Kijewska, A., Dzido, J. & Rokicki, J. (2009). Anisakis parasites of fishes caught on the African Shelf. Journal of Parasitology 95: 639–645. DOI: 10.1645/GE-1796.1.

Klimpel, S., Palm, H.W., Rückert, S. & Piatkowski, U. (2004). The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitology Research 94: 1–9. DOI: 10.1007/s00436-004-1154-0.

Klimpel, S. & Rückert, S. (2005). Life cycle strategy of Hysterothylacium aduncum to become the most abundant anisakid fish nematode in the North Sea. Parasitology Research 97: 141–149. DOI: 10.1007/s00436-005-1407-6.

Kuhn, T., García-Màrquez, J. & Klimpel, S. (2011). Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. Public Library of Science ONE 6: e28642. DOI: 10.1371/journal.pone.0028642.

Levsen, A., Paoletti, M., Cipriani, P., Nascetti, G. & Mattiucci, S. (2016). Species composition and infection dynamics of ascaridoid nematodes in Barents Sea capelin (Mallotus villosus) reflecting trophic position of fish host. Parasitology Research 115: 4281–4291. DOI: 10.1007/s00436-016-5209-9.

Link, J.S., Jason, S., Bogstad, B., Sparholt, H. & Lilly, G.R. (2009). Trophic role of Atlantic cod in the ecosystem. Fish and Fisheries 10: 1467–2979. DOI: 10.1111/j.1467-2979.2008.00295.x.

Marcogliese, D.J. (1996). Transmission of the sealworm, Pseudoterranova decipiens (Krabbe), from invertebrates to fish in an enclosed brackish pond. Journal of Experimental Marine Biology and Ecology 205: 205–219. DOI: 10.1016/S0022-0981(96)02613-5.

Margolis, L., Esch, G.W., Holmes, J.C., Kuris, A.M. & Shad, G.A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). Journal of Parasitology 68: 131–133. DOI:10.2307/3281335.

Martell, D.J. & McClelland, G. (1995). Transmission of Pseudoterranova decipiens (Nematoda: Ascaridoidea) via benthic macrofauna to sympatric flatfishes (Hippoglossoides platessoides, Pleuronectes ferrugineus, P. americanus) on Sable Island Bank, Canada. Journal of Marine Biology 122: 129–135. DOI: 10.1007/BF00349286.

Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P. et al. (1997). Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology 83: 401–416. DOI: 10.2307/3284402.

Mattiucci S., Paggi L., Nascetti G., Ishikura H., Kikuchi, K. et al. (1998). Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda: Ascaridoidea). Systematic Parasitology 40: 81–92. DOI: 10.1023/A:1005914926720.

McClelland G. (1995). Experimental infections of fish with larval sealworm, Pseudoterranova decipiens (Nematoda, Anisakinae), transmitted by amphipods. Canadian Journal of Fisheries and Aquatic Sciences 52: 140–155. DOI: 10.1139/f95-520.

McClelland, G., Misra, R.K. & Martell, D.J. (1985). Variations in abundance of larval anisakines, sealworm (Pseudoterranova decipiens) and related species, in eastern Canadian cod and flatfish. Canadian Technical Report of Fisheries and Aquatic Sciences No. 1392, p. 57.

McClelland, G., Misra, R.K. & Martell, D.J. (1990). Larval anisakine nematodes in various fish species from Sable Island Bank and vicinity. Canadian Bulletin of Fisheries and Aquatic Sciences 222: 83–113.

Michalsen, K. & Nedreaas, K.H. (1998). Food and feeding of Greenland halibut (Reinhardtius hippoglossoides, Walbaum) in the Barents Sea and East Greenland waters. Sarsia 83: 401–407. DOI: 10.1080/00364827.1998.10413699.

Mouritsen, K.N., Hedeholm, R., Schack, H.B., Møller, L.N., Storr-Paulsen, M. et al. (2010). Occurrence of anisakid nematodes in Atlantic cod (Gadus morhua) and Greenland cod (Gadus ogac), West Greenland. Acta Parasitologica 55(1): 81–89. DOI: 10.2478/s11686-010-0009-3.

Nascetti, G., Cianchi, R., Mattiucci, S., D’Amelio, S., Orecchia, P. et al. (1993). Three sibling species within Contracaecum osculatum (Nematoda, Ascaridida, Ascaridoidea) from the Atlantic Arctic-Boreal region: reproductive isolation and host preferences. International Journal of Parasitology 23(1): 105–120. DOI: 10.1016/0020-7519(93)90103-6.

Nedreaas, K.H. & Smirnov, O. (2004). Stock characteristics, fisheries and management of Greenland halibut (Reinhardtius hippoglossoides Walbaum) in the northeast Arctic. IMR/PINRO, Conference, 23p.

Orecchia, P., Mattiucci, S., D’Amelio, S., Paggi, L., Plötz, J. et al. (1994). Two new members in the Contracaecum osculatum complex (Nematoda, Ascaridoidea) from the Antarctic. International Journal of Parasitology 24(3): 367–377. DOI: 10.1016/0020-7519(94)90084-1.

Paggi, L., Nascetti, G., Cianchi, R., Orecchia, P., Mattiucci, S. et al. (1991). Genetic evidence for three species within Pseudoterranova decipiens (Nematoda, Ascaridida, Ascaridoidea) in the North Atlantic and Norwegian and Barents Seas. International Journal of Parasitology 21: 195–212. DOI: 10.1016/0020-7519(91)90010-5.

Palm, H.W. (1999). Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitology Research 85: 638–646. DOI: 10.1007/s004360050608.

Palsson, J. & Beverly-Burton, M. (1984). Helminth parasites of capelin, Mallotus villosus (Pisces: Osmeridae) of the north Atlantic. Proceedings of the Helminthological Society of Washington 51: 248–254.

Rodríguez-Marín, E., Punzón, A. & Paz, J. (1995). Feeding patterns of Greenland halibut (Reinhardtius hippoglossoides) in Flemish Pass (Northwest Atlantic). NAFO Scientific Council Studies 23: 43–54.

Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press: 2028 p.

Sato, K., Inoue, J. & Watanabe, M. (2014). Influence of the Gulf Stream on the Barents Sea ice retreat and Eurasian coldness during early winter. Environmental Research Letters 9: 084009. DOI: 10.1088/1748-9326/9/8/084009.

Smith, J.W. (1971). Thysanoessa inermis¬ and¬ T. longicaudata¬ (Euphausiidae) as first intermediate hosts of¬ Anisakis¬ sp. (Nematoda: Ascaridata) in the northern North Sea, to the north of Scotland and at Faroe. Nature 234: 478. DOI: 10.1038/234478a0.

Smith, J.W. (1983). Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) (Nematoda: Ascaridoidea): morphology and morphometry of larvae from euphausiids and fish, and a review of the life-history and ecology. Journal of Helminthology 57: 205–224. DOI: 10.1017/S0022149X00009512.

Smith, J.W. (1984). The abundance of Anisakis simplex L3 in the body cavity and flesh of marine teleosts. International Journal of Parasitology 14: 491–495. DOI: 10.1016/0020-7519(84)90030-4.

Sobecka, E., Łuczak, E., Wiecaszek, B. & Antoszek, A. (2011). Parasite community structure of cod from Bear Island (Barents Sea) and Pomeranian Bay (Baltic Sea). Polish Polar Research 32: 199–287. DOI: 10.2478/v10183-011-0016-6.

Volkov, D.L., Landerer, F.W. & Kirillov, S.A. (2013). The Genesis of sea level variability in the Barents Sea. Continental Shelf Research 66: 92-104. DOI: 10.1016/j.csr.2013.07.007.

Wierzbicka, J. (1992). Parasitic fauna of Greenland halibut, Reinhardtius hippoglossoides (Walbaum, 1792) from the Barents Sea. Acta Ichthyologica et Piscatoria 22: 31–37. DOI: 10.3750/AIP1992.22.1.03.

Zhu, X.Q., Gasser, R.B., Podolska, M. & Chilton, N.B. (1998). Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal of Parasitology 28: 1911–1921. DOI: 10.1016/S0020-7519(98)00150-7.

Zhu, X.Q., D’Amelio, S., Paggi, L. & Gasser, R.B. (2000). Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitology Research 86: 677–683. DOI: 10.1007/PL00008551.

Downloads

Published

2018-06-11

How to Cite

Najda, K., Kijewska, A., Kijewski, T., Plauška, K., & Rokicki, J. (2018). Distribution of ascaridoid nematodes (Nematoda: Chromadorea: Ascaridoidea) in fish from the Barents Sea. Oceanological and Hydrobiological Studies, 47(2), 128–139. Retrieved from https://czasopisma.bg.ug.edu.pl/index.php/oandhs/article/view/8617

Issue

Section

Articles