Cestodes of Antarctic and Subantarctic fish: History and prospects of research

Main Article Content

Polyakova T. A., Gordeev I. I. Cestodes of Antarctic and Subantarctic fish: History and prospects of research. Marine Biological Journal, 2020, vol. 5, no. 4, pp. 79-93. https://doi.org/10.21072/mbj.2020.05.4.07

Article Details

Abstract

The first information about cestodes of Antarctic and Subantarctic fish appeared at the beginning of the XX century: a cestode Phyllobothrium dentatum from an unknown shark was described. Peak of activity of studying Antarctic cestodes fell on 1990–2006. During this period, significant works were published, devoted to description of new species, their life cycles, host specificity of cestodes – fish parasites, and their geographical distribution. A notable contribution to the study of elasmobranch cestodes was made by a group of Polish scientists, headed by Wojciechowska (Rocka). Systematic position of 21 cestode species from 13 genera of 8 families of 6 orders was analyzed. Cestode fauna has been studied in less than 7 % of the total ichthyofauna of this area, while potential definitive and intermediate hosts remain unexplored. The largest number of cestode species (12) was recorded in four ray species of the family Rajidae. Eight cestode species, reaching sexual maturity, have been registered in intestines of teleosts: Bothriocephalus antarcticus, B. kerguelensis, Bothriocephalus sp., Parabothriocephalus johnstoni, P. macruri, Clestobothrium crassiceps, Neobothriocephalus sp., and Eubothrium sp. Larvae of five cestode species (Onchobothrium antarcticum, Grillotia (Grillotia) erinaceus, Lacistorhynchus tenuis, Calyptrobothrium sp., and Hepatoxylon trichiuri), ending their development in elasmobranchs, were found in teleosts. Systematic position of 5 cestode species out of 12, found in rays, is unidentified. Cestode fauna is characterized by a high level of endemism: 67 % of the total cestode fauna is not found to the north of Subantarctic. Coastal areas, mostly covered by research, are those in the Atlantic and Indian sectors of Antarctic. The biodiversity of elasmobranch cestodes, inhabiting Antarctic and Subantarctic, is underestimated, since only one third of species of these fish have been studied so far. Genetic studies of Antarctic cestodes have just begun to develop. Ribosomal sequences from D1–D3 fragments of 28S rDNA are known for 2 species only: Onchobothrium antarcticum from the second intermediate (Notothenia rossii and Dissostichus mawsoni) and definitive hosts (Bathyraja eatonii), as well as larvae of Calyptrobothrium sp. from the second intermediate hosts (D. mawsoni and Muraenolepis marmorata). The main directions of further research on cestode fauna should be developed in combination with morphological, faunistic, genetic, and ecological studies.

Authors

T. A. Polyakova
senior researcher, PhD

http://orcid.org/0000-0002-0071-1801

https://elibrary.ru/author_items.asp?id=892741

I. I. Gordeev
senior researcher, PhD

http://orcid.org/0000-0002-6650-9120

https://elibrary.ru/author_items.asp?id=504366

References

Гаевская А. В., Родюк Г. Н. Экологическая характеристика паразитофауны южноатлантического макруруса (Macrourus carinatus Gunther) // Биологические науки : научные доклады высшей школы. 1988. № 2. С. 21–25. [Gaevskaya A. V., Rodyuk G. N. The parasitofauna ecological characteristic of Macrourus carinatus Gunther. Biologicheskie nauki : nauchnye doklady vysshei shkoly, 1988, no. 2, pp. 21–25. (in Russ.)]

Гаевская А. В., Родюк Г. Н. Эколого-географические особенности паразитофауны угретресковых (Pisces: Muraenolepidae) // Экология моря. 1997. Вып. 46. С. 28–31. [Gaevskaya A. V., Rodjuk G. N. Ecological-geographical characters of parasite fauna of muraenolepids (Pisces: Muraenolepidae). Ekologiya morya, 1997, iss. 46, pp. 28–31. (in Russ.)]

Гаевская А. В., Родюк Г. Н., Парухин А. М. Особенности и формирование паразитофауны патагонского клыкача Dissostichus eleginoides // Биология моря. 1990. № 4. С. 23–28. [Gaevskaya A. V., Rodyuk G. N., Parukhin A. M. Peculiarities and formation of parasitofauna of the Patagonian toothfish Dissostichus eleginoides. Biologiya morya, 1990, no. 4, pp. 23–28. (in Russ.)]

Квач Ю., Кузьміна Т. Паразитологічні дослідження в Антарктиці: огляд проблематики та перспективи // Український антарктичний журнал. 2020. № 1. С. 102–110. [Kvach Y., Kuzmina T. Parasitological research in Antarctica: Review of the issues and future prospects. Ukrainskii Antarcticheskii Zhurnal, 2020, no. 1, pp. 102–110. (in Ukr.)]. https://doi.org/10.33275/1727-7485.1.2020.383

Лядов В. Н. Зоогеографическая характеристика гельминтов рыб Антарктической зоны Мирового океана // Симпозиум по паразитологии и патологии морских организмов, Ленинград, 13–16 октября 1981 г. : тезисы докладов советских участников. Ленинград : Наука, 1981. С. 58–61. [Lyadov V. N. Zoogeograficheskaya kharakteristika gel’mintov ryb Antarkticheskoi zony Mirovogo okeana. In: Simpozium po parazitologii i patologii morskikh organizmov, Leningrad, 13–16 Oct. 1981 : tezisy dokladov sovetskikh uchastnikov. Leningrad : Nauka, 1981, pp. 58–61. (in Russ.)]

Лядов В. Н., Парухин А. М., Миронова А. В. Гельминтофауна промысловых рыб семейства Chaenichthyidae из района островов Кергелен // Зоологический журнал. 1981. Т. 60, вып. 1. С. 142–144. [Lyadov V. N., Parukhin A. M., Mironova A. V. Helminth fauna of fishes of the family Chaenichthyidae from the region of Kergelen islands. Zoologicheskii zhurnal, 1981, vol. 60, iss. 1, pp. 142–144. (in Russ.)]

Парухин А. М. Особенности гельминтофауны промысловых нототениевых рыб Субантарктического сектора Индийского океана // Вестник зоологии. 1986. № 3. С. 6–10. [Parukhin A. M. Peculiarities of nototheniid fish helminth fauna in Subantarctic sector of Indian ocean. Vestnik zoologii, 1986, no. 3, pp. 6–10. (in Russ.)]

Парухин А. М., Лядов В. Н. Паразитофауна нототениевидных рыб (Notothenioidei) из вод Атлантического и Индийского океанов // Вестник зоологии. 1981. № 3. С. 90–94. [Parukhin A. M., Lyadov V. N. Parasitofauna of Notothenioidei from waters of the Atlantic and Indian oceans. Vestnik zoologii, 1981, no. 3, pp. 90–94. (in Russ.)]

Парухин А. М., Лядов В. Н. Гельминтофауна промысловых рыб семейства Nototheniidae Кергеленской подобласти // Экология моря. 1982. Вып. 10. С. 49–56. [Parukhin A. M., Lyadov V. N. Helminth fauna of food Nototheniidae fishes from Kerguelen subregion. Ekologiya morya, 1982, iss. 10, pp. 49–56. (in Russ.)]

Bargelloni L., Ritchie P. A., Patarnello T., Battaglia B., Lambert D. M., Meyer A. Molecular evolution at subzero temperatures: Mitochondrial and nuclear phylogenies of fishes from Antarctica (suborder Notothenioidei), and the evolution of antifreeze glycopeptides. Molecular Biology and Evolution, 1994, vol. 11, pp. 854–863. https://doi.org/10.1093/oxfordjournals.molbev.a040168

Brickle P., MacKenzie K., Pike A. Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the Subantarctic. Polar Biology, 2005, vol. 28, pp. 663–671. https://doi.org/10.1007/s00300-005-0737-2

Brickle P., MacKenzie K., Pike A. Variations in the parasite fauna of the patagonian toothfish (Dissostichus elegenoides Smitt, 1898), with length, season, and depth of habitat around the Falkland Islands. Journal of Parasitology, 2006, vol. 92, iss. 2, pp. 282–291. https://doi.org/10.1645/GE-539R.1

Caira J. N., Jensen K., Waeschenbach A., Olson P. D., Littlewood D. T. J. Orders out of chaos – Molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. International Journal for Parasitology, 2014, vol. 44, iss. 1, pp. 55–73. https://doi.org/10.1016/j.ijpara.2013.10.004

Campbell R. A., Correia S. J., Haedrich R. L. A new monogenean and cestode from the deep-sea fish, Macrourus berglax Lacépède, 1802, from the Flemish Cap off Newfoundland. Proceedings of the Helminthological Society of Washington, 1982, vol. 49, no. 2, pp. 169–175.

Dailey M. D., Vogelbein W. Clistobothrium carcharodoni gen. et sp. n. (Cestoda: Tetraphyllidea) from the spiral valve of the Great White Shark (Carcharodon carcharias). Journal of the Helminthological Society of Washington, 1990, vol. 57, no. 2, pp. 108–112.

de Meeus T., Renaud F. Parasites within the new phylogeny of eukaryotes. Trends in Parasitology, 2002, vol. 18, iss. 6, pp. 247–251. https://doi.org/10.1016/S1471-4922(02)02269-9

Dobson A., Lafferty K. D., Kuris A. M., Hechinger R. F., Jetz W. Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America, 2008, vol. 105, iss. 1, pp. 11482–11489. https://doi.org/10.1073/pnas.0803232105

Duhamel G., Hulley P.-A., Causse R., Koubbi P., Vacchi M., Pruvost P., Vigetta S., Irisson J.-O., Mormede S., Belchier M., Dettai A., Detrich H. W., Gutt J., Jones C. D., Kock K.-H., Lopez Abellan L. J., Van de Putte A. Biogeographic patterns of fish. In: Biogeographic Atlas of the Southern Ocean / C. De Broyer, P. Koubbi et al. (Eds). Cambridge, UK : Scientific Committee on Antarctic Research, 2014, chap. 7, pp. 328–362.

Eastman J. T. Antarctic Fish Biology: Evolution in a Unique Environment. San Diego : Academic Press, 1993, 322 p.

FishBase. World Wide Web electronic publication. Version (12.2019) : [official site], 2019. URL: https://www.fishbase.se/ [accessed: 02.09.2020].

Fonseca V. G., Carvalho G. R., Sung W., Johnson H. F., Power D. M., Neill S. P., Packer M., Blaxter M. L., Lambshead P. J. D., Thomas W. K., Creer S. Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nature Communications, 2010, vol. 1, art. no. 98 (8 p.). http://doi.org/10.1038/ncomms1095

Gordeev I., Polyakova T. Helminths and the stomach contentment of Bathyraja sp. (Rajiformes: Arhynchobatidae) in the Simushir Island area (Pacific Ocean). Journal of Asia-Pacific Biodiversity, 2020, vol. 13, iss. 2, pp. 306–309. https://doi.org/10.1016/j.japb.2020.03.005

Gordeev I. I., Sokolov S. G. Parasites of Antarctic toothfish Dissostichus mawsoni (Norman, 1937) (Perciformes, Nototheniidae). Polar Research, 2016, vol. 35, art. no. 29364 (5 p.). http://doi.org/10.3402/polar.v35.29364

Gordeev I. I., Sokolov S. G. Helminths and the feeding habits of the marbled moray cod Muraenolepis marmorata Günther, 1880 (Gadiformes, Muraenolepididae) in the Ross Sea (Southern Ocean). Polar Biology, 2017, vol. 40, iss. 6, pp. 1311–1318. http://doi.org/10.1007/s00300-016-2055-2

Ivanov V. A., Campbell R. A. Notomegarhynchus navonae n. gen. and n. sp. (Eucestoda: Teteraphyllidea), from skates (Rajidae: Arhynchobatinae) in the Southern Hemisphere. Journal of Parasitology, 2002, vol. 88, no. 2, pp. 340–349. https://doi.org/10.2307/3285586

Klimpel S., Kuhn T., Mehlhorn H. (Eds). Biodiversity and Evolution of Parasitic Life in the Southern Ocean. Cham, Switzerland : Springer International Publishing, 2017, 226 p. (Parasitology Research Monographs ; vol. 9).

Klimpel S., Palm H. W. Anisakid nematode (Ascaridoidea) life cycles and distribution: Increasing zoonotic potential in the time of climate change? In: Progress in Parasitology. Berlin ; Heidelberg : Springer, 2011, pp. 201–222. (Parasitology Research Monographs ; vol 2). https://doi.org/10.1007/978-3-642-21396-0_11

Kock K. H. Antarctic Fish and Fisheries. Cambridge : Cambridge University Press, 1992, 359 p.

Kuchta R., Scholz T. Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008. In: Planetary Biodiversity Inventory (2008–2017): Tapeworms From Vertebrate Bowels of the Earth / J. N. Caira, K. Jensen (Eds) ; University of Kansas, Natural History Museum. Landisville, Pennsylvania : Yurchak Printing, Inc., 2017, pp. 29–46. (Special Publication ; no. 25).

Kuchta R., Scholz T., Bray R. A. Revision of the order Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008 (Eucestoda) with amended generic diagnoses and keys to families and genera. Systematic Parasitology, 2008, vol. 71, iss. 2, pp. 81–136. https://doi.org/10.1007/s11230-008-9153-7

Kuzmina T. A., Salganskij O. O., Lisitsyna O. I., Korol E. M. 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, 2020, vol. 54, no. 2, pp. 99–110. http://doi.org/10.15407/zoo2020.02.099

Laskowski Z., Rocka A. Molecular identification larvae of Onchobothrium antarcticum Cestoda: Tetraphyllidea) from marbled rockcod, Notothenia rossii, in Admiralty Bay (King George Island, Antarctica). Acta Parasitlogica, 2014, vol. 59, iss. 4, pp. 767–772. https://doi.org/10.2478/s11686-014-0301-8

Laskowski Z., Rocka A., Zdzitowiecki K. New data on the occurrence of internal parasitic worms in the Gymnodraco acuticeps and Cygnodraco mawsoni (Bathydraconidae) fish in the Ross Sea, Antarctica. Polish Polar Research, 2005, vol. 26, no. 1, pp. 37–40.

Laskowski Z., Rocka A., Zdzitowiecki K., Ozouf-Costaz C. Occurrence of endoparasitic worms in dusky notothen, Trematomus newnesi (Actinopterygii Nototheniidae), at Adélie Land, Antarctica. Polish Polar Research, 2007, vol. 28, no. 1, pp. 37–42.

Lyadov V. N. Zoogeographical characteristics of the helminths of fishes from the Antarctic zone of the World Ocean. In: Parasitology and Pathology of Marine Organisms of the World Ocean / H. S. Hargis, Jr. (Ed.). Seattle, Washington : US Department of Commerce, 1985, pp. 41–43. (NOAA Technical Report NMFS ; vol. 25).

Muñoz G., Cartes F. D. Endoparasitic diversity from the Southern Ocean: Is it really low in Antarctic fish? Journal of Helminthology, 2020, vol. 94, art. no. e180. https://doi.org/10.1017/S0022149X20000590

Münster J., Kochmann J., Klimpel S., Klapper R., Kuhn T. Parasite fauna of Antarctic Macrourus whitsoni (Gadiformes: Macrouridae) in comparison with closely related macrourids. Parasites & Vectors, 2016, vol. 9, art. no. 403 (11 p.). http://doi.org/10.1186/s13071-016-1688-x

Oğuz M. C., Tepe Y., Belk M. C., Heckmann R. A., Aslan B., Gürgen M., Bray R. A., Akgül Ü. Metazoan parasites of Antarctic fishes. Türkiye Parazitoloji Derneği, 2015, vol. 39, no. 2, pp. 174–178. http://doi.org/10.5152/tpd.2015.3661

Palm H. W., Reimann N., Spindler M., Plötz J. The role of the rock cod Notothenia coriiceps Richardson, 1844 in the life-cycle of Antarctic parasites. Polar Biology, 1998, vol. 19, iss. 6, pp. 399–406. https://doi.org/10.1007/s003000050265

Palm H. W., Klimpel S., Walter T. Demersal fish parasite fauna around the South Shetland Islands: High species richness and low host specificity in deep Antarctic waters. Polar Biology, 2007, vol. 30, iss. 12, pp. 1513–1522. https://doi.org/10.1007/s00300-007-0312-0

Poulin R., Morand S. Diversity of parasites. The Quarterly Review of Biology, 2000, vol. 75, no. 3, pp. 277–293. https://doi.org/10.1086/393500

Poulin R., Morand S. Parasite biodiversity. Washington, DC : Smithsonian Institution Books, 2004, 216 p.

Prudhoe S. Cestodes from fish, birds and whales. Reports (British Australian and New Zealand Antarctic Research Expedition 1929–1931, Ser. B.), 1969, vol. 8, pt. 9, pp. 171–193.

Reimer L. W., Jessen O. Ein Beitrag zur Parasitenfauna von Merluccius hubbsi Marini. Wissenschaftsbereich Zoologie Pädagogischen Hochschule Güstrow, 1974, vol. 2, pp. 53–64.

Rocka A. Cestodes of the Antarctic fishes. Polish Polar Research, 2003, vol. 24, no. 3–4, pp. 261–276.

Rocka A. Helminths of Antarctic fishes: Life cycle biology, specificity, and geographical distribution. Acta Parasitologica, 2006, vol. 51, iss. 1, pp. 26–35. https://doi.org/10.2478/s11686-006-0003-y

Rocka A. Cestodes and nematodes of Antarctic fishes and birds. In: Biodiversity and Evolution of Parasitic Life in the Southern Ocean / S. Klimpel, T. Kuhn, H. Mehlhorn (Eds). Cham, Switzerland : Springer, 2017, chap. 6, pp. 77–107. (Parasitology Research Monographs ; vol. 9). http://doi.org/10.1007/978-3-319-46343-8

Rocka A., Zdzitowiecki K. Cestodes in fishes of the Weddell Sea. Acta Parasitologica, 1998, vol. 43, pp. 64–70.

Ruhnke T. R., Caira J. N., Pickering M. Phyllobothriidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. In: Planetary Biodiversity Inventory (2008–2017): Tapeworms From Vertebrate Bowels of the Earth / J. N. Caira, K. Jensen (Eds) ; University of Kansas, Natural History Museum. Landisville, Pennsylvania : Yurchak Printing, Inc., 2017, pp. 305–326. (Special Publication ; no. 25).

Santoro M., Mattiucci S., Work T., Cimmaruta R., Nardi V., Cipriani P., Bellisario B., Nascetti G. Parasitic infection by larval helminths in Antarctic fishes: Pathological changes and impact on the host body condition index. Diseases of Aquatic Organisms, 2013, vol. 105, no. 2, pp. 139–148. http://doi.org/10.3354/dao02626

Southwell T. A Monograph on the Tetraphyllidea With Notes on Related Cestodes. Liverpool : University Press of Liverpool, Ltd. ; London : Hodder and Stoughton, Ltd., 1925, 368 p. (Memoirs of the Liverpool School of Tropical Medicine, New Series ; no. 2).

Walter T., Palm H. W., Piepiorka S., Rückert S. Parasites of the Antarctic rattail Macrourus whitsoni (Regan, 1913) (Macrouridae, Gadiformes). Polar Biology, 2002, vol. 25, iss. 9, pp. 633–640. https://doi.org/10.1007/s00300-002-0407-6

Wojciechowska A. Onchobothrium antarcticum sp. n. (Tetraphyllidea) from Bathyraja eatonii (Günther, 1876) and a plerocercoid from Notothenioidea (South Shetlands, Antarctic). Acta Parasitologica Polonica, 1990a, vol. 35, no. 2, pp. 113–117.

Wojciechowska A. Pseudanthobothrium shetlandicum sp. n. and P. notogeorgianum sp. n. (Tetraphyllidea) from rays in the regions of the South Shetlands and South Georgia (Antarctic). Acta Parasitologica Polonica, 1990b, vol. 35, no. 3, pp. 181–186.

Wojciechowska A. New species of the genus Phyllobothrium (Cestoda, Tetraphyllidea) from Antarctic batoid fishes. Acta Parasitologica Polonica, 1991a, vol. 36, no. 2, pp. 63–68.

Wojciechowska A. Some tetraphyllidean and diphyllidean cestodes from Antarctic batoid fishes. Acta Parasitologica Polonica, 1991b, vol. 36, no. 2, pp. 69–74.

Wojciechowska A. The tetraphyllidean and tetrabothriid cercoids from Antarctic bony fishes. I. Morphology. Identification with adult forms. Acta Parasitologica, 1993a, vol. 38, no. 1, pp. 15–22.

Wojciechowska A. The tetraphyllidean and tetrabothriid cercoids from Antarctic bony fishes. II. Occurrence of cercoids in various fish species. Acta Parasitologica, 1993b, vol. 38, no. 3, pp. 113–118.

Wojciechowska A. The tetraphyllidean and tetrabothriid cercoids from Antarctic bony fishes. III. Infection of Notothenia neglecta and N. rossii in Admiralty Bay. Acta Parasitologica, 1993c, vol. 38, no. 4, pp. 166–169.

Wojciechowska A., Zdzitowiecki K., Pisano E., Vacchi M. The tetraphyllidean cercoids from bony fishes occurring in the Ross Sea (Antarctic). Acta Parasitologica, 1994, vol. 39, no. 1, pp. 13–15.

Wojciechowska A., Pisano E., Zdzitowiecki K. Cestodes in fishes at the Heard Island (Subantarctic). Polish Polar Research, 1995, vol. 16, pp. 205–212.

Yamaguti S. Systema Helminthum. Vol. II. The Cestodes of Vertebrates. New York : Interscience Publishers, 1959, 860 p.

Zdzitowiecki K. New data on the occurrence of fish endoparasitic worms off Adelie Land, Antarctica. Polish Polar Research, 2001, vol. 22, no. 2, pp. 159–165.

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

Zdzitowiecki K., Zadrozny T. Endoparasitic worms of Harpagifer antarcticus off the South Shetland Islands (Antarctic). Acta Parasitologica, 1999, vol. 44, no. 2, pp. 125–130.

Zdzitowiecki K., White M. G., Rocka A. Digenean, monogenean, and cestode infection of inshore fish at the South Orkney Islands. Acta Parasitologica, 1997, vol. 42, no. 1, pp. 18–22.

Zdzitowiecki K., Rocka A., Pisano E., Ozouf-Costaz C. A list of fish parasitic worms collected off Adélie Land (Antarctica). Acta Parasitologica, 1998, vol. 43, no. 2, pp. 71–74.

Statistics

Downloads

Download data is not yet available.