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In situ evidence of the role of Crangon crangon in infection of cod Gadus morhua with nematode parasite Hysterothylacium aduncum in the Baltic Sea
Published online by Cambridge University Press: 09 August 2021
Abstract
Cod was one of the most important fish species in the Baltic Sea, but its condition is deteriorating for several reasons, including an increasing parasite burden. The aim of this study was to determine the source of infection of Baltic cod with parasites by examination of invertebrates found in situ in the cod stomach. A total of 1681 cod were sampled during four research cruises in the southern Baltic Sea in 2012, 2013 and 2014 and the composition of their diet was analysed. Each prey item from cod stomach was identified to the lowest possible taxonomic level and a parasitological analysis of all invertebrates collected was performed. Crangon crangon, Saduria entomon and Mysis mixta were the most commonly represented invertebrates among food items. Hysterothylacium aduncum was found only in C. crangon. This host–parasite system is reported here for the first time in situ in the stomach of cod from the Baltic Sea, confirming the role of C. crangon in cod infection with H. aduncum.
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- Copyright © National Marine Fisheries Research Institute, 2021. Published by Cambridge University Press
References
Abdel-Ghaffar, F, Abdel-Gaber, R, Bashtar, AR, Morsy, K, Mehlhorn, H, Al Quraishy, S and Saleh, R (2015) Hysterothylacium aduncum (Nematoda, Anisakidae) with a new host record from the common sole Solea solea (Soleidea) and its role as a biological indicator of pollution. Parasitology Research 114, 513–522.CrossRefGoogle Scholar
Adroher, FJ, Malagon, D, Valero, A and Benitez, R (2004) In vitro development of the fish parasite Hysterothylacium aduncum from the third larval stage recovered from a host to the third larval stage hatched from the egg. Diseases of Aquatic Organisms 58, 41–45.CrossRefGoogle Scholar
Andersen, K (1993) Hysterothylacium aduncum (Rudolphi, 1862) infection in cod from the Oslofjord: seasonal occurrence of third- and fourth-stage larvae as well as adult worms. Parasitology Research 79, 67–72.CrossRefGoogle ScholarPubMed
Aro, E (2000) The spatial and temporal distribution patterns of cod (Gadus morhua callarias L.) in the Baltic Sea and their dependence on environmental variability – implications for fishery management (Dissertation). University of Helsinki.Google Scholar
Berland, B (1961) Nematodes from some Norwegian marine fishes. Sarsia 2, 1–52.CrossRefGoogle Scholar
Berland, B (1989) Identification of larval nematodes from fish. In Möller H. (eds). Nematode problems in North Atlantic fish. Report from a workshop in Kiel, 3–4 April 1989. ICES, C.M./F6, pp. 16–22.Google Scholar
Buchmann, K (1995) Ecological implications of Echinorhynchus gadi parasitism of Baltic cod (Gadus morhua). Journal of Fish Biology 46, 539–540.CrossRefGoogle Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Carstensen, J, Andersen, JH, Gustafsson, BG and Conley, DJ (2014) Deoxygenation of the Baltic Sea during the last century. Proceedings of the National Academy of Sciences 111, 5628–5633.CrossRefGoogle ScholarPubMed
Conley, DJ, Bj̈orck, S, Bonsdorff, E, Carstensen, J, Destouni, G, Gustafsson, BG, Hietanen, S, Kortekaas, M, Kuosa, H, Meier, HEM, Müller-Karulis, B, Nordberg, K, Norkko, A, Nürnberg, G, Pitkänen, H, Rabalais, NN, Rosenberg, R, Savchuk, OP, Slomp, CP, Voss, M, Wulff, F and Zillén, L (2009) Hypoxia-related processes in the Baltic Sea. Environmental Science & Technology 43, 3412–3420.CrossRefGoogle ScholarPubMed
Deardorff, TL and Overstreet, RM (1981) Review of Hysterothylacium and Iberingascaris (both previously Thynnascaris) (Nematoda: Anisakidae) from the northern gulf of Mexico. Proceedings of the Biological Society of Washington 93, 1035–1079.Google Scholar
Dural, M, Genc, E, Sangun, MK and Güner, Ö (2011) Accumulation of some heavy metals in Hysterothylacium aduncum (Nematoda) and its host sea bream, Sparus aurata (Sparidae) from North-Eastern Mediterranean Sea (Iskenderun Bay). Environmental Monitoring and Assessment 174, 147–155.CrossRefGoogle Scholar
Eero, M, Vinther, M, Haslob, H, Huwer, B, Casini, M, Storr-Paulsen, M and Koster, FW (2012) Spatial management of marine resources can enhance the recovery of predators and avoid local depletion of forage fish. Conservation Letters 5, 486–492.CrossRefGoogle Scholar
Engelhardt, J, Frisell, O, Gustavsson, H, Hansson, T, Sjoberg, R, Collier, TK and Balk, L (2020) Severe thiamine deficiency in eastern Baltic cod (Gadus morhua). PLoS ONE 15, e0227201.CrossRefGoogle Scholar
Fagerholm, HP (1982) Parasites of fish in Finland. VI. Nematodes. Acta Academiae Aboensis Series B 40, 1–128.Google Scholar
Ghadam, M, Banaii, M, Mohammed, ET, Suthar, J and Shamsi, S (2018) Morphological and molecular characterization of selected species of Hysterothylacium (Nematoda: Raphidascarididae) from marine fish in Iraqi waters. Journal of Helminthology 92, 116–124.CrossRefGoogle ScholarPubMed
Gibson, DI (1972) Flounder parasites as biological tags. Journal of Fish Biology 4, 1–9.CrossRefGoogle Scholar
Haarder, S, Kania, PW, Galatius, A and Buchmann, K (2014) Increased Contracaecum osculatum infection in Baltic cod (Gadus morhua) livers (1982–2012) associated with increasing grey seal (Halichoerus gryphus) populations. Journal of Wildlife Diseases 50, 537–543.CrossRefGoogle ScholarPubMed
Hayward, PJ and Ryland, JS (1995) Handbook of the Marine Fauna of North-West Europe. Oxford: Oxford University Press.Google Scholar
Hemmingsen, W and MacKenzie, K (2001) The parasite fauna of the Atlantic cod, Gadus morhua L. Advances in Marine Biology 40, 1–80.CrossRefGoogle Scholar
Horbowy, J, Podolska, M and Nadolna-Ałtyn, K (2016) Increasing occurrence of Anisakid nematodes in the liver of cod (Gadus morhua) from the Baltic Sea: does infection affect the condition and mortality of fish? Fisheries Research 179, 98–103.CrossRefGoogle Scholar
Hurst, RJ (1984) Marine invertebrate hosts of New Zealand Anisakidae (Nematoda). New Zealand Journal of Marine and Freshwater Research 18, 187–196.CrossRefGoogle Scholar
ICES (2019) Cod (Gadus morhua) in subdivisions 24–32, eastern Baltic stock (eastern Baltic Sea). In Report of the ICES Advisory Committee, cod.27.24-32. https://doi.org/10.17895/ices.advice.4747.CrossRefGoogle Scholar
Iglesias, L, Valero, A, Galvez, L, Benitez, R and Adroher, FJ (2002) In vitro cultivation of Hysterothylacium aduncum (Nematoda: Anisakidae) from 3rd-stage larvae to egg-laying adults. Parasitology 125, 467–475.CrossRefGoogle ScholarPubMed
Jackson, CJ, Marcogliese, DJ and Burt, MDB (1997) Role of hyperbenthic crustaceans in the transmission of marine helminth parasites. Canadian Journal of Fisheries and Aquatic Sciences 54, 815–820.CrossRefGoogle Scholar
Khan, RA and Chandra, CV (2006) Influence of climatic changes on the parasites of Atlantic cod Gadus morhua off coastal Labrador, Canada. Journal of Helminthology 80, 193.CrossRefGoogle ScholarPubMed
Klimpel, S and Ruckert, S (2005) Life cycle strategies of Hysterothylacium aduncum to become the most abundant Anisakid fish nematode in the North Sea. Parasitology Research 97, 141–149.CrossRefGoogle Scholar
Knoff, M, Felizardo, NN, Iñiguez, AM, Maldonado, A Jr, Torres, EJL, Pinto, RM and Gomes, DC (2012) Genetic and morphological characterisation of a new species of the genus Hysterothylacium (Nematoda) from Paralichthys isosceles Jordan, 1890 (Pisces: Teleostei) of the Neotropical Region, state of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 107, 186–193.CrossRefGoogle ScholarPubMed
Køie, M (1993) Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Canadian Journal of Zoology 71, 1289–1296.CrossRefGoogle Scholar
Køie, M and Fagerholm, HP (1995) The life cycle of Contracaecum osculatum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea, Anisakidae) in view of experimental infection. Parasitology Research 81, 481–489.CrossRefGoogle Scholar
Kong, Q, Fan, L, Zhang, J, Akao, N, Dong, K, Lou, D, Ding, J, Tong, Q, Zheng, B, Chen, R, Ohta, N and Lu, S (2015) Molecular identification of Anisakis and Hysterothylacium larvae in marine fishes from the East China Sea and the Pacific coast of central Japan. International Journal of Food Microbiology 199, 1–7.CrossRefGoogle ScholarPubMed
Lick, R (1991) Investigations concerning the life cycle (crustaceans – fish – marine mammals) and freezing tolerance of Anisakine nematodes in the North Sea and the Baltic Sea (in German). (PhD thesis). Christian-Albrechts-Universität, Kiel.Google Scholar
Lindegren, M, Möllmann, C, Nielsen, A and Stenseth, NC (2009) Preventing the collapse of the Baltic cod stock through an ecosystem-based management approach. Proceedings of the National Academy of Sciences 106, 14722–14727.CrossRefGoogle ScholarPubMed
Marcogliese, DJ (1995) The role of zooplankton in the transmission of helminth parasites to fish. Reviews in Fish Biology and Fisheries 5, 336–371.CrossRefGoogle Scholar
Marcogliese, DJ (1996) Larval parasitic nematodes infecting marine crustaceans in eastern Canada. 3. Hysterothylacium aduncum. Journal of the Helminthological Society of Washington 63, 12–18.Google Scholar
Mehrdana, F, Bahlool, QZM, Skov, J, Marana, MH, Sindberg, D, Mundeling, M, Overgaard, , Korbut, R, Strom, SB, Kania, PW and Buchmann, K (2014) Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod (Gadus morhua) from the Baltic Sea. Veterinary Parasitology 205, 581–587.CrossRefGoogle ScholarPubMed
Mellergaard, S and Lang, T (1999) Diseases and parasites of Baltic cod (Gadus morhua) from the Mecklenburg Bright to the Estonian coast. ICES Journal of Marine Science 56, 164–168.CrossRefGoogle Scholar
Moravec, F and Nagasawa, TN (1986) New records of amphipods as intermediate hosts for salmonid nematode parasites in Japan. Folia Parasitologica 33, 45–49.Google Scholar
Moravec, F, Taraschewski, H, Appelhoff, D and Weyl, O (2012) A new species of Hysterothylacium (Nematoda: Anisakidae) from the giant mottled eel Anguilla marmorata in South Africa. Helminthologia 49, 174–180.CrossRefGoogle Scholar
Morsy, K, Bashtar, AR, Mostafa, N, El Deeb, S and Thabet, S (2015) New host records of three juvenile nematodes in Egypt: Anisakis sp. (type II), Hysterothylacium patagonense (Anisakidae), and Echinocephalus overstreeti (Gnathostomatidae) from the greater lizard fish Saurida undosquamis of the Red Sea. Parasitology Research 114, 1119–1128.CrossRefGoogle ScholarPubMed
Münster, J, Klimpel, S, Fock, HO, MacKenzie, K and Kuhn, T (2015) Parasites as biological tags to track an ontogenetic shift in the feeding behaviour of Gadus morhua off West and East Greenland. Parasitology Research 114, 2723–2733.CrossRefGoogle ScholarPubMed
Myjak, P, Szostakowska, B, Wojciechowski, J, Pietkiewicz, H and Rokicki, J (1994) Anisakidae larvae in cod from the southern Baltic Sea. Archive of Fishery and Marine Research 42, 149–161.Google Scholar
Nadolna, K and Podolska, M (2014) Anisakid larvae in the liver of cod (Gadus morhua) L. from the southern Baltic Sea. Journal of Helminthology 88, 237–246.CrossRefGoogle ScholarPubMed
Navone, GT, Sardella, NH and Timi, JT (1998) Larvae and adult of Hysterothylacium aduncum (Nematoda: Anisakidae) in fishes and crustaceans in the South West Atlantic. Parasite 5, 127–136.CrossRefGoogle ScholarPubMed
Norris, DE and Overstreet, RM (1976) The Public Health Implications of Larval Thvnnesceris Nematodes from Shellfish. Journal of Milk and Food Technology 39, 47–54.CrossRefGoogle Scholar
Pachur, ME and Horbowy, J (2013) Food composition and prey selection of cod, Gadus morhua (Actinopterygii: Gadiformes: Gadidae), in the southern Baltic Sea. Acta Ichthyologica et Piscatoria 43, 109–118.CrossRefGoogle Scholar
Pawlak, J, Nadolna-Ałtyn, K, Szostakowska, B, Pachur, M and Podolska, M (2018) Saduria entomon infected with Hysterothylacium aduncum found in situ in the stomach of cod (Gadus morhua) from the Baltic Sea. Journal of Helminthology 92, 645–648.CrossRefGoogle ScholarPubMed
Pawlak, J, Nadolna-Ałtyn, K, Szostakowska, B, Pachur, M, Bańkowska, A and Podolska, M (2019) First evidence of the presence of Anisakis simplex in Crangon crangon and Contracaecum osculatum in Gammarus sp. by in situ examination of the stomach contents of cod (Gadus morhua) from the southern Baltic Sea. Parasitology 146, 1699–1706.CrossRefGoogle ScholarPubMed
Pekmezci, GZ, Bolukbas, CS, Gurler, AT and Onuk, EE (2013) Occurrence and molecular characterization of Hysterothylacium aduncum (Nematoda: Anisakidae) from Merlangius merlangus euxinus and Trachurus trachurus off the Turkish coast of Black Sea. Parasitology Research 112, 1031–1037.CrossRefGoogle ScholarPubMed
Perdiguero-Alonso, D, Montero, FE, Raga, JA and Kostadinova, A (2008) Composition and structure of the parasite faunas of cod, Gadus morhua L. (Teleostei: Gadidae), in the North East Atlantic. Parasites & Vectors 1, 23.CrossRefGoogle Scholar
Pilecka-Rapacz, M and Sobecka, E (2004) Parasites of young Baltic cod, Gadus morhua callarias L. in the Gulf of Puck, Poland. Acta Ichthyologica et Piscatoria 34, 235–240.CrossRefGoogle Scholar
Rello, FJ, Adroher, FJ and Valero, A (2008) Hysterothylacium aduncum, the only Anisakid parasite of sardines (Sardina pilchardus) from the southern and eastern coasts of Spain. Parasitology Research 104, 117–121.CrossRefGoogle Scholar
Roca-Geronès, X, Montoliu, I, Godínez-González, C, Fisa, R and Shamsi, S (2018) Morphological and genetic characterization of Hysterothylacium Ward & Magath, 1917 (Nematoda: Raphidascarididae) larvae in horse mackerel, blue whiting and anchovy from Spanish Atlantic and Mediterranean waters. Journal of Fish Diseases 41, 1463–1475.CrossRefGoogle ScholarPubMed
Rokicki, J (2009) Effects of climatic changes on Anisakid nematodes in polar regions. Polar Science 3, 197–201.CrossRefGoogle Scholar
Saulamo, K and Neuman, E (2002) Local management of Baltic fish stocks – significance of migrations. Fiskeriverket Informerar 9, 1–18.Google Scholar
Shamsi, S (2017) Morphometric and molecular descriptions of three new species of Hysterothylacium (Nematoda: Raphidascarididae) from Australian marine fish. Journal of Helminthology 91, 613.CrossRefGoogle ScholarPubMed
Shamsi, S, Poupa, A and Justine, JL (2015) Characterisation of ascaridoid larvae from marine fish off New Caledonia, with description of new Hysterothylacium larval types XIII and XIV. Parasitology International 64, 397–404.CrossRefGoogle ScholarPubMed
Shamsi, S, Ghadam, M, Suthar, J, Mousavi, HE, Soltani, M and Mirzargar, S (2016) Occurrence of ascaridoid nematodes in selected edible fish from the Persian Gulf and description of Hysterothylacium larval type XV and Hysterothylacium persicum n. sp. (Nematoda: Raphidascarididae). International Journal of Food Microbiology 236, 65–73.CrossRefGoogle Scholar
Shamsi, S, Steller, E and Chen, Y (2018) New and known zoonotic nematode larvae within selected fish species from Queensland waters in Australia. International Journal of Food Microbiology 272, 73–82.CrossRefGoogle ScholarPubMed
Skrzypczak, M and Rolbiecki, L (2015) Endoparasitic helminths of the European Sprat, Sprattus sprattus (Linnaeus, 1758) from the Gulf of Gdańsk (the Southern Baltic Sea) with a checklist of its parasites. Russian Journal of Marine Biology 41, 167–175.CrossRefGoogle Scholar
Svendsen, YS (1990) Hosts of third stage larvae of Hysterothylacium sp. (Nematoda, Anisakidae) in zooplankton from outer Oslofjord, Norway. Sarsia 75, 161–167.CrossRefGoogle Scholar
Szaniawska, A (1991) Energy management in benthic invertebrates from the Baltic Sea (PhD thesis). Publication of Gdańsk University Press (in Polish).Google Scholar
Szostakowska, B, Myjak, P, Wyszyński, M, Pietkiewicz, H and Rokicki, J (2005) Prevalence of anisakin nematodes in fish from Southern Baltic Sea. Polish Journal of Microbiology 54, 41–45.Google ScholarPubMed
Unger, P and Palm, HW (2016) Parasitation of sea trout (Salmo trutta trutta L.) from the spawning ground and German coastal waters off Mecklenburg-Western Pomerania, Baltic Sea. Parasitology Research 115, 165–174.CrossRefGoogle ScholarPubMed
Valtonen, ET and Julkunen, M (1995) Influence of the transmission of parasites from prey fishes on the composition of the parasite community of a predatory fish. Canadian Journal of Fisheries and Aquatic Sciences 52, 233–245.CrossRefGoogle Scholar
Zander, CD (2004) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic. Parasitology Research 93, 17–29.CrossRefGoogle Scholar
Zander, CD, Strohbach, U and Groenewotd, S (1993) The importance of gobies (Gobiidae, Teleostei) as hosts and transmitters of parasites in the SW Baltic. Helgoländer Meeresuntersuchungen 47, 81–111.CrossRefGoogle Scholar
Zander, CD, Groenewold, S and Strohbach, U (1994) Parasite transfer from crustacean to fish hosts in the Lubeck Bight, SW Baltic Sea. Helgoländer Meeresuntersuchungen 48, 89–105.CrossRefGoogle Scholar
Zander, CD, Reimer, LW, Barz, K, Dietel, G and Strohbach, U (2000) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea) II. Guild communities, with special regard to snails, benthic crustaceans, and small-sized fish. Parasitology Research 86, 359–372.CrossRefGoogle ScholarPubMed
Zhu, X, Gasser, RB, Podolska, M and Chilton, NB (1998) Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal for Parasitology 28, 1911–1921.CrossRefGoogle ScholarPubMed
Żmudziński, L (1961) Skorupiaki dziesięcionogie (Decapoda) Bałtyku [Decapods of the Baltic Sea]. Przegląd Zoologiczny 5, 352–360 (in Polish).Google Scholar
Żmudziński, L (1967) Zoobentos Zatoki Gdańskiej [Zoobenthos of Gulf of Gdańsk]. Publication of MIR 16A, 47–80 (in Polish).Google Scholar
Żmudziński, L (1990) Świat zwierzęcy Bałtyku: atlas makrofauny [Animal world of the Baltic Seas: atlas of Macrofauna] Wydawnictwa Szkolne i Pedagogiczne Warszawa, 195 pp. (in Polish).Google Scholar
Zuo, S, Huwer, B, Bahlool, , Al-Jubury, A, Christensen, ND, Korbut, R, Kania, P and Buchmann, K (2016) Host size-dependent anisakid infection in Baltic cod Gadus morhua associated with differential food preferences. Diseases of Aquatic Organism 120, 69–75.CrossRefGoogle ScholarPubMed