Ukrainian Antarctic journal

Vol 20 No 1(24) (2022): Ukrainian Antarctic Journal
Articles

Analysis of the helminth community of Notothenia coriiceps (Actinopterygii: Nototheniidae) collected in the water area of the Argentine Islands, West Antarctica

T. Kuzmina
I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Kyiv, 01030, Ukraine
Yu. Kuzmin
I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Kyiv, 01030, Ukraine; African Amphibian Conservation Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom, 2520, South Africa
O. Salganskiy
National University of Life and Environmental Sciences of Ukraine, Kyiv, 03041, Ukraine
O. Lisitsyna
I. I. Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, Kyiv, 01030, Ukraine
E. Korol
National Museum of Natural History, National Academy of Sciences of Ukraine, Kyiv, 01030, Ukraine
Published August 4, 2022
Keywords
  • Antarctic black rockcod,
  • component community,
  • diversity indices,
  • infracommunity,
  • species richness

Abstract

Helminth community of the Antarctic black rockcod, Notothenia coriiceps, was examined using the fish samples collected in 2014—2015 (106 specimens) and 2020—2021 (78 specimens) in the water area of the Argentine Islands, West Antarctica. In total, 30,951 helminth specimens were collected and identified. We analyse the helminth infra- and component communities and investigate possible changes in the main parameters of helminth communities of N. coriiceps during the six-year period. Thirty species of helminths from five taxonomic groups were recorded: one species of Monogenea, 5 of Nematoda, 4 of Cestoda, 9 of Trematoda, and 11 of Acanthocephala. Notothenia coriiceps was found to be the definitive host of 18 helminth species; 12 species parasitize it in the larval stage using N. coriiceps as the second intermediate or paratenic host. The proportion of larval helminths in the samples was lower in 2014—2015 (73.4%) than in 2020—2021 (81.4%). The number of dominant helminth species (infection prevalence >50%) increased from seven in 2014—2015 to nine in 2020—2021. In helminth infracommunities, the species richness was similar in two samples. On the other hand, we found significantly higher helminth abundance in the infracommunities from the sample collected in 2020—2021. In the helminth component community, the diversity indices (Shannon, Simpson, Pielou, Berger-Parker) evidenced higher evenness and lower domination in the sample collected in 2014—2015 compared to the sample collected in 2020—2021. Lower evenness in 2020—2021 was due to the larger relative abundance of larval Pseudoterranova sp. and Corynosoma spp. We suggest a deeper investigation of the role of separate helminth species in the component community changes, as well as further monitoring of component community parameters as prospective directions for future studies of helminth communities of N. coriiceps in West Antarctica.

References

  1. Alt, K. G., Cunze, S., Kochmann, J., & Klimpel, S. (2021). Parasites of three closely related Antarctic fish species (Teleostei: Nototheniinae) from Elephant Island. Acta Parasitologica, 67, 218—232. https://doi.org/10.1007/s11686-021-00455-8
  2. Amin, O. M. (2013). Classification of the Acanthocephala. Folia Parasitologica (Praha), 60(4), 273—305. https://doi.org/10.14411/fp.2013.031
  3. Amin, O. M., Heckmann, R. A., Dallarés, S., Constenla, M., Rubtsova, N. Yu., & Kuzmina, T. (2021). New perspectives on Aspersentis megarhynchus (Acanthocephala: Heteracanthocephalidae) from Notothenia coriiceps Richardson (Nototheniidae) in the West Antarctic, with emended generic diagnosis. Journal of Helminthology, 95, E27, 1—14. https://doi.org/10.1017/S0022149X2100016X
  4. Barrera-Oro, E. (2002). The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula, Antarctic Science, 14(4), 293—309. https://doi.org/10.1017/S0954102002000111
  5. Barrera-Oro, E., & Casaux, R. (1990). Feeding selectivity in Notothenia neglecta, Nybelin, from Potter Cove, South Shetland Islands, Antarctica. Antarctic Science, 2(3), 207—213. https://doi.org/10.1017/S0954102090000281
  6. 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. https://doi.org/10.2307/3284227
  7. Casaux, R., & Barrera-Oro, E. (2013). Dietary overlap in inshore notothenioid fish from the Danco Coast, Western Antarctic Peninsula. Polar Research, 32(1), 1—8. https://doi.org/10.3402/polar.v32i0.21319
  8. Chapman, J. M., Marcogliese, D. J., Suski, C. D., & Cooke, S. J. (2015). Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat quality. Ecological Indicators, 57, 564—572. https://doi.org/10.1016/j.ecolind.2015.05.013
  9. Clarke, K. R., & Gorley, R. N. (2006). PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E.
  10. Coggan, R. (1997). Seasonal and annual growth rates in the Antarctic fish Notothenia coriiceps Richardson. Journal of Experimental Marine Biology and Ecology, 213(2), 215—229. https://doi.org/10.1016/S0022-0981(96)02731-1
  11. Drago, F. B. (2012). Community structure of metazoan parasites of silverside, Odontesthes bonariensis (Pisces, Atherinopsidae) from Argentina. Iheringia, Séria Zoologica, 102(1), 26—32. https://doi.org/10.1590/S0073-47212012000100004
  12. Faltýnková, A., Kudlai, O., Salganskij, O. O., Korol, E. M., & Kuzmina, T. A. (2022). Trematodes from Antarctic teleost fishes off Argentine Islands, West Antarctica: molecular and morphological data. Systematic Parasitology, 99(4), 491—523. https://doi.org/10.1007/s11230-022-10041-9
  13. George-Nascimento, M., & Oliva, M. (2015). Fish population studies using parasites from the South-Eastern Pacific Ocean: considering host population changes and species body size as sources of variability of parasite communities. Parasitology, 142(1), 25—35. https://doi.org/10.1017/S0031182014001127
  14. Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 4.
  15. 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
  16. Iken, K., Barrera-Oro, E., Quartino, M., Casaux, R., & Brey, T. (1997). Grazing by the Antarctic fish Notothenia coriiceps: evidence for selective feeding on macroalgae. Antarctic Science, 9(4), 386—391. https://doi.org/10.1017/S0954102097000497
  17. Klimpel, S., Seehagen, A., Palm, H. W., & Rosenthal, H. (2001). Deep-water metazoan fish parasites of the world. Logos.
  18. Klimpel, S., Kuhn, T., & Mehlhorn, H. (2017). Introduction: Biodiversity and evolution of parasitic life in the Southern Ocean. In S. Klimpel, T. Kuhn, & H. Mehlhorn (Eds.) Biodiversity and evolution of parasitic life in the Southern Ocean. Parasitology Research Monographs (Vol. 9, pp. 1—5), Springer. https://doi.org/10.1007/978-3-319-46343-8_1
  19. Klöser, H., Plötz, J., Palm, H., Bartsch, A., & Hubold, G. (1992). Adjustment of anisakid nematode life cycles to the high Antarctic food web as shown by Contracaecum radiatum and C. osculatum in the Weddell Sea. Antarctic Science, 4(2), 171—178. https://doi.org/10.1017/S0954102092000269
  20. 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
  21. Kuzmina, T. A., Dykyy, I. V., Salganskij, O. O., Lisitsyna, O. I., Korol, E. M., & Kuzmin, Yu. I. (2021a). 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
  22. Kuzmina, T. A., Salganskij, O. O., Dykyy, I. V., Lisitsyna, O. I., Korol, E. M., Faltýnková, A., & Kuzmin, Y. I. (2021b). Helminths of the Antarctic dragonfish, Parachaenichthys charcoti (Perciformes, Notothenioidei, Bathydraconidae) studied near Galindez Island (Argentine Islands, West Antarctica). Acta Parasitologica, 66(4), 1424—1430. https://doi.org/10.1007/s11686-021-00417-0
  23. Kuzmina, T. A., Laskowski, Z., Salganskij, O. O., Zdzi towiecki, K., Lisitsyna, O. I., & Kuzmin, Y. (2022a). Helminth assemblages of the Antarctic black rockcod, Notothenia coriiceps (Actinopterygii: Nototheniidae) in coastal waters near Galindez Island (Argentine Islands, West Antarctic): temporal changes in the endoparasite community. Acta Parasitologica, 67(1), 207—217. https://doi.org/10.1007/s11686-021-00448-7
  24. Kuzmina, T. A., Salganskij, O. O., Vishnyakova, K. O., Ivanchikova, J., Lisitsyna, O. I., Korol, E. M., & Kuzmin, Y. I. (2022b). Helminth diversity in teleost fishes from the South Orkney Islands region, West Antarctica. Zoodiversity, 56(2), 135—152. https://doi.org/10.15407/zoo2022.02.135
  25. Kvach, Y., & Kuzmina, T. (2020). Parasitological research in Antarctica: review of the issues and future prospects. Ukrainian Antarctic Journal, 1, 102—110. https://doi.org/10.33275/1727-7485.1.2020.383. (In Ukrainian)
  26. La Mesa, M., Eastman, J. T., & Vacchi, M. (2004). The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biology, 27, 321—338. https://doi.org/10.1007/s00300-004-0599-z
  27. 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.
  28. MacKenzie, K. (2002). Parasites as biological tags in population studies of marine organisms: an update. Parasitology, 124, 153—163. https://doi.org/10.1017/s0031182002001518
  29. Manilo, L. G. (2006). Ichthyofauna and morphobiological characteristics of mass fish species of coastal waters of Argentine Islands (Antarctica). Zbirnyk prats Zoologichnogo Muzeju, 38, 5—22. (In Ukrainian)
  30. Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology, 124(7), 83—99. https://doi.org/10.1017/s003118200200149x
  31. Marcogliese, D. J., & Jacobson, K. (2015). Parasites as biological tags of marine, fresh water and anadromous fishes in North America from the tropics to the Arctic. Parasitology, 142(1), 68—89. https://doi.org/10.1017/S0031182014000110
  32. McCormack, S. A., Melbourne-Thomas, J., Trebilco, R., Blanchard, J. L., Raymond, B., & Constable, A. (2021). Decades of dietary data demonstrate regional food web structures in the Southern Ocean. Ecology and Evolution, 11(1), 227—241. https://doi.org/10.1002/ece3.7017
  33. Möller, H. (1987). Pollution and parasitism in the aquatic environment. International Journal for Parasitology, 17(2), 353—361. https://doi.org/10.1016/0020-7519(87)90110-X
  34. 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. The Journal of parasitology, 77(4), 551—556. https://doi.org/10.2307/3283158
  35. Mouritsen, K. N., & Poulin, R. (2002). Parasitism, climate oscillations and the structure of natural communities. Oikos, 97(3), 462—468. https://doi.org/10.1034/j.1600-0706.2002.970318.x
  36. 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
  37. 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
  38. Near, T. J. (2009). Notothenioid fishes (Notothenioidei). In S. B. Hedges, & S. Kumar (Eds.) The timetree of life (pp. 339—343). Oxford University Press.
  39. Near, T. J., Dornburg, A., Kuhn, K. L., Eastman, J. T., Pennington, J. N., Patarnello, T., Zane, L., Fernández, D. A., & Jones, C. D. (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
  40. 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. Turkish Journal of Parasitology, 39, 174—178. https://doi.org/10.5152/tpd.2015.3661
  41. Palm, H. W. (1999). Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitology Research, 85(8—9), 638—46. https://doi.org/10.1007/s004360050608
  42. 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
  43. Palm, H. W., Klimpel, 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, 1513—1522. https://doi.org/10.1007/s00300-007-0312-0
  44. Polyanski, Y. I. (1961). Ecology of parasites of marine fishes. In V. A. Dogiel, G. K. Petrushuvski, & Y. I. Polyanski (Eds.) Parasitology of Fishes (pp. 48—83). Oliver and Boyd.
  45. Poulin, R. (2019). Best practice guidelines for studies of parasite community ecology. Journal of Helmintholohy, 93(1), 8—11. https://doi.org/10.1017/S0022149X18000767
  46. 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
  47. 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
  48. Trokhymets, V. M., Tymofyeyev, V. A., & Perechrest, J. S. (2010). The fish fauna of the Argentine Islands region (Antarctica; 12 UAE 2007—2008) and morphometrical changeability of Notothenia coriiceps (Richardson, 1844). Ukrainian Antarctic Journal, 6, 206—214. https://doi.org/10.33275/1727-7485.9.2010.407
  49. Weber, E. P. 3rd, & Govett, P. (2009). Parasitology and necropsy of fish. Compendium on Continuing Education for the Practising Veterinarian, 31(2), E12.
  50. Williams, H. H., MacKenzie, K., & McCarthy, A. M. (1992). Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries, 2, 144—176.
  51. Zdzitowiecki, K., & Laskowski, Z. (2004). Helminths of an Antarctic fish, Notothenia coriiceps, from the Vernadsky Station (Western Antarctic) in comparison with Admirality Bay (South Shetland Islands). Helminthologia, 41, 201—207.