Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica

  • T. Kuzmina I. I. Schmalhausen Institute of Zoology NAS of Ukraine
  • I. V. Dykyy Zoological Museum of Lviv National University, 4, Grushevsky Street, Lviv, 79005, Ukraine
  • O. O. Salganskij
  • O. I. Lisitsyna I. I. Schmalhausen Institute of Zoology NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukraine
  • E. M. Korol National Museum of Natural History NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukra
  • Yu. I. Kuzmin I. I. Schmalhausen Institute of Zoology NAS of Ukraine; 15, Bogdan Khmelnytskyi Street, Kyiv, 01030, Ukraine
Keywords: Helminths, Acanthocephala, Nematoda, Cestoda, Trematoda, teleost fishes, Antarctica

Abstract

Monitoring studies of the species diversity in marine ecosystems provide important data on ecological changes caused by global warming and anthropogenic influence. The present work was aimed to analyze the species diversity of the helminths parasitic in teleost fishes inhabiting the area near the Ukrainian Antarctic Station "Akademik Vernadsky" (Galindez Island, Argentine Islands, West Antarctica). During April – January of 2014–2015 and 2019–2020, 156 specimens of six fish species (Notothenia coriiceps, N. rossii, Chaenocephalus aceratus, Parachaenichthys charcoti, Trematomus bernacchii, and Harpagifer antarcticus) were examined. Totally, 21,166 specimens of 31 helminth species were collected and assigned to five taxonomic groups: Monogenea (1 species), Digenea (10), Nematoda (5), Cestoda (4), and Acanthocephala (11). Twenty-six helminth species were found in N. coriiceps,14 in N. rossii, 27 in P. charcoti, 23 in Ch. aceratus, 16 in T. bernacchii, and six in H. antarcticus. Larval stages of anisakid nematodes prevailed in helminth community of Ch. aceratus (66%) and P. charcoti (40%), while other fish species were mostly infected with acanthocephalans, trematodes and cestodes. The present data on the species diversity of helminth communities can be used as a baseline for long-term monitoring studies of fish parasites in the region of Argentine Islands.

References

Anderson, R. C. 2000. Nematode Parasites of Vertebrates. Their Development and Transmission. Second Edition. CABI Publishing, Wallingford, 1-650.

https://doi.org/10.1079/9780851994215.0000

Barnes, D. K. A., Peck, L. S. 2008. Vulnerability of Antarctic shelf biodiversity to predicted regional warming. Climate Research, 37 (2-3), 149-163.

https://doi.org/10.3354/cr00760

Barrera-Oro, E., Moreira, E., Seefeldt, M. A., Mariano. V. F., Quartino, M. L. 2019. The importance of macroalgae and associated amphipods in the selective benthic feeding of sister rockcod species Notothenia rossii and N. coriiceps (Nototheniidae) in West Antarctica. Polar Biology, 42 (2), 317-334.

https://doi.org/10.1007/s00300-018-2424-0

Brickle, P., MacKenzie, K., Pike, A. 2005. Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the Subantarctic. Polar Biology, 28 (9), 663-671.

https://doi.org/10.1007/s00300-005-0737-2

Busch, M. W., Kuhn, T., Munster, J., Klimpel, S. H. 2012. Marine Crustaceans as Potential Hosts and Vectors for Metazoan Parasites. In: Mehlhorn, H. ed. Arthropods as Vectors of Emerging Diseases. Parasitology Research Monographs 3, Springer-Verlag Berlin Heidelberg, 239-360.

https://doi.org/10.1007/978-3-642-28842-5_14

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

https://doi.org/10.2307/3284227

Chown, S. L., Clarke, A., Fraser, C. I., Cary, S. C., Moon, K. L., McGeoch, M. A. 2015. The changing form of Antarctic biodiversity. Nature, 522 (7557), 431-438.

https://doi.org/10.1038/nature14505

Clarke, K. R., Gorley, R. N. 2006. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth.

Clarke, A., Johnston, N. M., Murphy, E. J., Rogers, A. D. 2007. Introduction: Antarctic ecology from genes to ecosystems: the impact of climate change and the importance of scale. Philosophical Transactions of the Royal Society, B, 362, 5-9.

https://doi.org/10.1098/rstb.2006.1943

Daszak, P., Cunningham, A. A., Hyatt, A. D. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica, 78 (2), 103-116.

https://doi.org/10.1016/S0001-706X(00)00179-0

De Broyer, C., Koubbi, P., Griffihs, H. J., Raymond, B., Udekem d'Acoz, C. d', Van de Putte, A. P., Danis, B., David, B., Grant, S., Gutt, J., Held, C., Hosie, G., Huettmann, F., Post, A., Ropert-Coudert, Y. (eds.), 2014. Biogeographic Atlas of the Southern Ocean. Scientifi Committee on Antarctic Research, Cambridge, 1-498.

Eastman, J. T. 1991. Evolution and diversification of Antarctic notothenioid fishes. American Zoologist, 31 (1), 93-109.

https://doi.org/10.1093/icb/31.1.93

Faltýnková, A., Georgieva, S., Kostadinova, A., Bray, R. A. 2017. Biodiversity and Evolution of Digeneans of Fishes in the Southern Ocean. In: Klimpel S., Kuhn T., Mehlhorn H., eds. Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Parasitology Research Monographs, vol 9. Springer, Cham, 49-75.

https://doi.org/10.1007/978-3-319-46343-8_5

Gibson, D. I., Jones, A., Bray, R. A. 2002. Keys to the Trematoda. Volume 1. CABI & Natural History Museum, Wallingford, UK, 1-544.

https://doi.org/10.1079/9780851995472.0000

Gordeev, I. I., Sokolov, S. G. 2016. Parasites of the Antarctic toothfish (Dissostichus mawsoni Norman, 1937) (Perciformes, Nototheniidae) in the Pacific sector of the Antarctic. Polar Research, 35, 29364.

https://doi.org/10.3402/polar.v35.29364

Hammer, Ø., Harper, D. A. T., Ryan, P. D. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4, 9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

Hudson, P. J., Dobson, A. P., Lafferty, K. D. 2006. Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution, 21 (7), 381-385.

https://doi.org/10.1016/j.tree.2006.04.007

Jones, A., Bray, R. A., Gibson, D. I. 2005. Keys to the Trematoda. Volume 2. CABI & Natural History Museum, Wallingford, UK, 1-768.

https://doi.org/10.1079/9780851995878.0000

Khan, R. A., Thulin. J. 1991. Influence of pollution on parasites of aquatic animals. Advances in Parasitology, 30,201-239.

https://doi.org/10.1016/S0065-308X(08)60309-7

Klapper, R., Münster, J., Kochmann, J., Klimpel, S., Kuhn, T. 2017. Biodiversity and Host Specificity of Monogenea in Antarctic Fish Species. In: Klimpel S. et al. (eds.) Biodiversity and Evolution of Parasitic Life in the Southern Ocean, Parasitology Research Monographs, Vol. 9, 33-47.

https://doi.org/10.1007/978-3-319-46343-8_4

Kock, K.-H. 1992. Antarctic fish and fisheries. Cambridge University Press, 1-359.

Kuhn, T., Zizka, V. M. A., Münster, J., Klapper, R., Mattiucci, S., Kochmann, J., Klimpel, S. 2018. Lighten up the dark: metazoan parasites as indicators for the ecology of Antarctic crocodile icefish (Channichthyidae) from the north-west Antarctic Peninsula. PeerJ. 6: e4638.

https://doi.org/10.7717/peerj.4638

Kuzmina, T. A., Salganskij, O. O., Lisitsyna, O. I., Korol, E. M. 2020. Helminths of Antarctic rockcod Notothenia coriiceps (Perciformes, Nototheniidae) from the Akademik Vernadsky Station area (Argentine Islands, West Antarctica): new data on the parasite community. Zoodiversity, 54 (2), 99-110.

https://doi.org/10.15407/zoo2020.02.099

Kvach, Y., Kuzmina, T. 2020. Parasitological research in Antarctica: review of the issues and future prospects. Ukrainian Antarctic Journal, 1, 102-110 [In Ukrainian].

https://doi.org/10.33275/1727-7485.1.2020.383

Laskowski, Z., Zdzitowiecki, K. 2005. The helminth fauna of some notothenioid fishes collected from the shelf of Argentine Islands, West Antarctica. Polish Polar Research, 26 (4), 315-324.

Laskowski, Z., Korczak-Abshire, M., Zdzitowiecki, K. 2012. Changes in acanthocephalan infection of the Antarctic fish Notothenia coriiceps in Admiralty Bay, King George Island, over 29 years. Polish Polar Research, 33 (1), 99-108.

https://doi.org/10.2478/v10183-012-0005-4

Laskowski, Z., Zdzitowiecki, K. 2017. Acanthocephalans in Sub-Antarctic and Antarctic. In: Klimpel S., Kuhn T., Mehlhorn H. (eds) Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Parasitology Research Monographs, vol 9. Springer, Cham, 141-182.

https://doi.org/10.1007/978-3-319-46343-8_8

Laskowski, Z., Rocka, A., Zdzitowiecki, K., Ozouf-Costaz, C. 2007. Occurrence of endoparasitic worms in dusky notothen, Trematomus newnesi (Actinopterygii Nototheniidae), at Adelie Land, Antarctica. Polish Polar Research, 28(1):37-42.

Manilo, L. G. 2006. Ichthyofauna and morphobiological characteristics of mass fish species of coastal waters of Argentine Islands (Antarctica). Zbirnyk prats Zoologichnogo Muzeyu 38 (1), 5-22 [In Ukrainian].

McKenna, J. E. Jr. 1991. Trophic relationships within the Antarctic demersal fish community of South Georgia Island. Fishery bulletin U.S., 89 (4), 643-654.

MacKenzie, K. 2017. The history of Antarctic parasitological research. In Klimpel, S., Kuhn, T., Mehlhorn, H. (eds). Biodiversity and evolution of parasitic life in the Southern Ocean, Parasitology Research Monographs, Vol. 9. Cham: Springer Nature, 13-31.

Moser, M., Cowen, R. K. 1991. The effects of periodic eutrophication on parasitism and stock identification of Trematomus bernacchii (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Journal of Parasitology, 77 (4), 551-556.

https://doi.org/10.2307/3283158

Mouritsen, K. N., Poulin, R. 2002. Parasitism, climate oscillations and the structure of natural ommunities. Oikos, 97 (3), 462-468.

https://doi.org/10.1034/j.1600-0706.2002.970318.x

Mozgovoy, A. A. 1951. Ascaridata of animals and man, and the diseases caused by them. Osnovy nematodologii. Vol. II. Izd-vo AN SSSR, Moskva, 1-616 [In Russian].

Muñoz, G., Cartes, F. D. 2020. Endoparasitic diversity from the Southern Ocean: is it really low in Antarctic fish? Journal of Helminthology 94, e180, 1-10.

https://doi.org/10.1017/S0022149X20000590

Muñoz, G., Rebolledo, M. 2019. Comparison of the parasite community of two notothens, Notothenia rossii and N. coriiceps (Pisces: Nototheniidae), from King George Island, Antarctica. Journal of Helminthology, 93 (6), 732-737.

https://doi.org/10.1017/S0022149X18000858

Münster, J., Kochmann, J., Grigat, J., Klimpel, S., Kuhn T. 2017. Parasite fauna of the Antarctic dragonfish Parachaenichthys charcoti (Perciformes: Bathydraconidae) and closely related Bathydraconidae from the Antarctic Peninsula, Southern Ocean. Parasites Vectors, 10, 235.

https://doi.org/10.1186/s13071-017-2176-7

Near, T. J. 2009. Notothenioid fishes (Notothenioidei). In: Hedges S.B., S. Kumar (Eds.), The Timetree of Life. Oxford University Press, 339-343.

Near, T. J., Dornburg, A., Kuhn, K. L., Eastman, J. T., Pennington, J. N., Patarnello, T., Zane, L., Fernández DA, Jones CD. 2012. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proceedings of the National Academy of Sciences of the United States of America, 109 (9), 3434-3439.

https://doi.org/10.1073/pnas.1115169109

Oğuz, M. C., Heckmann, R. A., Cheng, C. H. C., El-Naggar, A., Tepe, Y. 2012. Ecto and endoparasites of some fishes from the Antarctic Region. Scientia Parasitologica, 13 (3), 119-128.

Oğuz, M. C., Tepe, Y., Belk, M. C., Heckmann, R. A., Aslan, B., Gürgen, M., Bray, R. A., Akgül, Ü. 2015. Metazoan parasites of Antarctic fishes. Türkiye Parazitoloji Derneği, 39, 174-178.

https://doi.org/10.5152/tpd.2015.3661

Palm, H. W., Reimann, N., Spindler, M., Plötz, J. 1998. The role of the rock cod Notothenia coriiceps (Richardson, 1844) in the life-cycle of Antarctic parasites. Polar Biology, 19 (6), 399-406.

https://doi.org/10.1007/s003000050265

Palm, H. W., Klimpe, S., Walter, T. 2007. Demersal fish parasite fauna around the South Shetland Islands; high species richness and low host specificity in deep Antarctic waters. Polar Biology, 30 (12), 1513-1522.

https://doi.org/10.1007/s00300-007-0312-0

Parukhin, A. M. 1986. Helminthofauna peculiarities of commercial Nototheniodei from the SubAntarktic region of the Indian Ocean. Vestnik Zoologii, 3, 6-10.

Parukhin, A. M., Lyadov, V. N. 1982. Helminth fauna of food Nototheniidae fishes from Kerguelen subregion. Ekologija Morya, Kiev, 10, 49-57 [In Russian].

Poulin, R. 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology, 132(1), 143-151.

https://doi.org/10.1017/S0031182005008693

Poulin, R., Mouritsen, K.N. 2006. Climate change, parasitism and the structure of intertidal ecosystems. Journal of Helminthology, 80 (2), 183-191.

https://doi.org/10.1079/JOH2006341

Reid, W. D. K., Clarke, S., Collins, M. A., Belchier, M. 2007. Distribution and ecology of Chaenocephalus aceratus (Channichthyidae) around South Georgia and Shag Rocks (Southern Ocean). Polar Biology, 30(12), 1523-1533.

https://doi.org/10.1007/s00300-007-0313-z

Rocka, A. 1999. Biometrical variability and occurrence of Ascarophis nototheniae (Nematoda, Cystidicolidae), a parasitic nematode of Antarctic and subantarctic fishes. Acta Parasitologica, 44 (4), 188-192.

Rocka, A. 2003. Cestodes of the Antarctic Fishes. Polish Polar Research, 24 (4), 261-276.

Rocka, A. 2004. Nematodes of the Antarctic fishes. Polish Polar Research, 25 (2), 135-152.

Rocka, A. 2006. Helminths of Antarctic fishes: Life cycle biology, specificity and geographical distribution. Acta Parasitologica, 51 (1), 26-35.

https://doi.org/10.2478/s11686-006-0003-y

Rocka, A. 2017. Cestodes and Nematodes of Antarctic Fishes and Birds. In: Klimpel S., Kuhn T., Mehlhorn H. (eds) Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Parasitology Research Monographs, vol 9. Springer, Cham, 77-107.

https://doi.org/10.1007/978-3-319-46343-8_6

Rocka, A., Zdzitowiecki, K. 1998. Cestodes in Fishes of the Weddell Sea. Acta Parasitologica, 43 (1), 64-70.

Rokicki, J., Rodjuk, G., Zdzitowiecki, K. 2009. Larval ascaridoid nematodes (Anisakidae) in fish from the South Shetland Islands (Southern Ocean). Polish Polar Research, 30 (1), 49-58.

Siegel, V. 1980. Quantitative investigations on parasites of Antarctic Channichthyid and Nototheniid fishes. Meeresforschung, 28, 146-256.

Sokolov S. G., Gordeev I. I. 2016. Paralepidapedon variabile sp. n. (Trematoda, Lepocreadioidea, Lepidapedidae) and other representatives of the genus Paralepidapedon from Antarctic fish. Biology Bulletin, 43 (7), 612-618.

https://doi.org/10.1134/S1062359016070189

Sokolov, S. G., Gordeev I. I., Atopkin D. M. 2016. Redescription of trematode Gonocerca muraenolepisi Parukhin et Lyadov 1979 (Hemiuroidea, Derogenidae), a body cavity parasite of Antarctic fishes, with a discussion of its phylogenetic position. Invertebrate Zoology, 13 (2), 191-202.

https://doi.org/10.15298/invertzool.13.2.02

Sokolov S. G., Lebedeva D. I., Gordeev I. I., Khasanov F. K. 2019. Zdzitowieckitrema incognita gen. et sp. nov. (Trematoda, Xiphidiata) from the Antarctic fish Muraenolepis marmorata Günther, 1880 (Gadiformes: Muraenolepidae): ordinary morphology but unclear family affiliation. Marine Biodiversity, 49, 451-462.

https://doi.org/10.1007/s12526-017-0830-0

Swan D. C. 1936. Berlese's Fluid: Remarks upon its Preparation and use as a Mounting Medium. Bulletin of Entomological Research, 27 (03), 389-391.

https://doi.org/10.1017/S0007485300058259

Utevsky, А. 2007. Antarctic Piscicolid Leeches. Bonner Zoologische Monographien, 54, 1-80.

Veselskyy, M. V., Khoetskyy, P. B. 2018. Ichthyofauna of the waters of the archipelago of the Argentine Islands (Ukrainian Antarctic expedition 2015-2016). Naukovi Zapysky Ternopilskogo Natsionalnogo Pedagigichnogo Universytety, Seria Biologia, 1 (72), 36-43.

Weber, E. P. 3rd, Govett, P. 2009. Parasitology and necropsy of fish. Compendium on Continuing Education for the Practising Veterinarian, 31 (2). E12.

Wojciechowska, A. 1993. The tetraphyllidean and tetrabothriid cercoids from Antarctic bony fishes. I. Morphology. Identification with adult forms. Acta Parasitologica, 38 (1), 15-22.

Zdzitowiecki, K. 1979. Digenetic trematodes in alimentary tracts of fishes of south Georgia and South Shetland Islands (Antarctica). Acta Ichthyologica et Piscatoria, 9 (1), 15-30.

https://doi.org/10.3750/AIP1979.09.1.02

Zdzitowiecki, K. 1983. Antarctic acanthocephalans of the genus Metacanthocephalus. Acta Parasitologica Polonica, 28 (4), 417-437.

Zdzitowiecki, K. 1984 a. Some Antarctic acanthocephalans of the genus Corynosoma parasitizing Pinnipedia, with descriptions of three new species. Acta Parasitologica Polonica, 29 (4), 359-377.

Zdzitowiecki, K. 1984 b. Redescription of Corynosoma hamanni (Linstow, 1892) and description of C. pseudohamanni sp. n. (Acanthocephala) from the environs of the South Shetlands (Antarctic). Acta Parasitologica Polonica, 29 (4), 379-393.

Zdzitowiecki, K. 1986. Acanthocephala of the Antarctic. Polish Polar Research, 7 (1-2), 97-117.

Zdzitowiecki, K. 1987. Acanthocephalans of marine fishes in the regions of South Georgia and South Orkneys (Antarctic). Acta Parasitologica Polonica, 31 (4), 211-217.

Zdzitowiecki, K. 1991. Occurrence of digeneans in open sea fishes off the South Shetland Islands and South Georgia, and a list of fish digeneans in the Antarctic. Polish Polar Research, 12 (1), 55-72.

Zdzitowiecki, K. 1996. Acanthocephala in fish in the Weddell Sea (Antarctica). Acta Parasitologica, 41 (3), 199-203.

Zdzitowiecki, K. 2001. Occurrence of endoparasitic worms in fish, Parachaenichthys charcoti (Bathydraconidae), off the South Shetland Islands (Antarctica). Acta Parasitologica, 46 (1), 18-23.

Zdzitowiecki, K. 2002. Occurrence of Digenea in fishes of the family Nototheniidae in the Weddell Sea. Acta Parasitologica, 47 (3), 154-158.

Zdzitowiecki, K. 2003. Occurrence of Digenea in fishes other than Notothenioidei in the Weddell Sea and the whole Antarctica. Acta Parasitologica, 48 (3), 195-199.

Zdzitowiecki, K., Cielecka, D. 1997 a. Digenea of fishes of the Weddell Sea. II. The Genus Macvicaria (Opecoelidae). Acta Parasitologica; 42 (2), 77-83.

Zdzitowiecki, K., Cielecka, D. 1997 b. Digenea of fishes of the Weddell Sea. III. The Lepocreadiidae (genera Neolepidapedon and Lepidapedon), parasites of Notothenioidea, Acta Parasitologica, 42 (2), 84-91.

Zdzitowiecki, K. 1998. Diversity of Digenea, parasites of fishes in various areas of the Antarctic. In: Di Prisco, G., Pisano, E., Clarke, A., (eds.) Fishes of Antarctica. Milano: Springer, 87-94.

https://doi.org/10.1007/978-88-470-2157-0_7

Zdzitowiecki, K., Laskowski, Z. 2004. Helminths of an Antarctic fish, Notothenia coriiceps, from the Vernadsky Station (Western Antarctica) in comparison with Admiralty Bay (South Shetland Islands). Helminthologia, 41 (4), 201-207.

Zdzitowiecki, K., Ozouf-Costaz, C. 2013. Contribution to the knowledge of the parasitic fauna of fish off Adelie Land, Antarctica. Polish Polar Research, 34 (4), 429-435.

https://doi.org/10.2478/popore-2013-0023

Zdzitowiecki, K., White, M. G. 1992. Digenean Trematoda infection of inshore fish at South Georgia. Antarctic Science, 4 (1), 51-55.

https://doi.org/10.1017/S0954102092000105

Zdzitowiecki, K., White, M. G. 1996. Acanthocephalan infection of insore fishes at the South Orkney Islands. Antarctic Science, 8 (3), 273-276.

https://doi.org/10.1017/S0954102096000387

Zdzitowiecki, K., Zadrozny, T. 1999. Endoparasitic worms of Harpagifer antarcticus Nybelin, 1947 off the South Shetland Islands (Antarctic). Acta Parasitologica, 44, 125-130.

Published
2021-05-04
How to Cite
Kuzmina, T., Dykyy, I. V., Salganskij, O. O., Lisitsyna, O. I., Korol, E. M., & Kuzmin, Y. I. (2021). Helminth Diversity in Teleost Fishes from the Area of the Ukrainian Antarctic Station “Akademik Vernadsky”, Argentine Islands, West Antarctica . Zoodiversity, 55(3), 251–264. https://doi.org/10.15407/zoo2021.03.251
Section
Parasitology