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Parasites in Antarctic krill guts inferred from DNA sequences

Published online by Cambridge University Press:  10 January 2019

Alison C. Cleary*
Affiliation:
University of Rhode Island Graduate School of Oceanography
Maria C. Casas
Affiliation:
University of Rhode Island Graduate School of Oceanography
Edward G. Durbin
Affiliation:
University of Rhode Island Graduate School of Oceanography
Jaime Gómez-Gutiérrez
Affiliation:
Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas

Abstract

The keystone role of Antarctic krill, Euphausia superba Dana, in Southern Ocean ecosystems, means it is essential to understand the factors controlling their abundance and secondary production. One such factor that remains poorly known is the role of parasites. A recent study of krill diet using DNA analysis of gut contents provided a snapshot of the parasites present within 170 E. superba guts in a small area along the West Antarctic Peninsula. These parasites included Metschnikowia spp. fungi, Haptoglossa sp. peronosporomycetes, Lankesteria and Paralecudina spp. apicomplexa, Stegophorus sp. nematodes, and Pseudocollinia spp. ciliates. Of these parasites, Metschnikowia spp. fungi and Pseudocollinia spp. ciliates had previously been observed in E. superba, as had other genera of apicomplexans, though not Lankesteria and Paralecudina. In contrast, nematodes had previously only been observed in eggs of E. superba, and there are no literature reports of peronosporomycetes in euphausiids. Pseudocollinia spp., parasitoids which obligately kill their host, were the most frequently observed infection, with a prevalence of 12%. The wide range of observed parasites and the relatively high frequency of infections suggest parasites may play a more important role than previously acknowledged in E. superba ecology and population dynamics.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2019 

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Footnotes

*

Present address Norwegian Polar Institute

References

Altschul, S.F., Gih, W., Miller, W., Myers, E.W. & Lipman, D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215, 403410.Google Scholar
Cleary, A.C. & Durbin, E.G. 2016. Unexpected prevalence of parasite 18S rDNA sequences in winter among Antarctic marine protists. Journal of Plankton Research, 38, 401417.Google Scholar
Cleary, A.C., Durbin, E.G. & Casas, M.C. 2018. Feeding by Antarctic krill, Euphausia superba, in the West Antarctic Peninsula: differences between fjords and open waters. Marine Ecology Progress Series, 595, 10.3354/meps12568.Google Scholar
Diaz, J.I., Fusaro, B., Longarzo, L., Coria, N.R., Vidal, V., D'Amico, V., et al . 2016. Gastrointestinal helminths of Adélie penguins (Pygoscelis adeliae) from Antarctica. Polar Research, 35, 10.3402/polar.v35.28516.Google Scholar
Donachie, S.P. & Zdanowski, M.K. 1998. Potential digestive function of bacteria in krill Euphausia superba stomach. Aquatic Microbial Ecology, 14, 129136.Google Scholar
Eren, A.M., Morrison, H.G., Lescaut, P.J., Reveillaud, J., Vineis, J.H. & Sogin, M.L. 2015. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. The ISME Journal, 9, 968979.Google Scholar
Gómez-Gutiérrez, J. & Kawaguchi, S. 2017. Review: Pseudocollinia histophagous ciliates that infect krill in the Pacific and Atlantic oceans and possibly worldwide. CICIMAR Oceánides, 32, 1524.Google Scholar
Gómez-Gutiérrez, J., Kawaguchi, S., Morales-Ávila, J.R. 2017. Bacteria. In Gómez-Gutiérrez, J., Kawaguchi, S. & Morales-Ávilaeds, J.R., eds. Global diversity and ecological function of parasites of euphausiids. Cham: Springer, 214 pp.Google Scholar
Gómez-Gutiérrez, J., López-Cortez, A., Aguilar-Méndez, M.J., Del Angel-Rodríguez, J., Tremblay, N., Zenteno-Savín, T., et al . 2015. Histophagous ciliate Pseudocollinia brintoni and bacterial assemblage interaction with krill Nyctiphanes simplex: I. Transmission process. Diseases of Aquatic Organisms, 16, 10.3354/dao02922. Google Scholar
Gómez-Gutiérrez, J. & Morales-Ávila, J.R. 2016. Parasites and diseases. In Siegel, V., ed. Biology and ecology of Antarctic krill. Cham: Springer, 441 pp. 10.1007/978-3-319-29279-3_10.Google Scholar
Gómez-Gutiérrez, J., Peterson, W.T., De Roberetis, A. & Brodeur, R.D. 2003. Mass mortality of krill caused by parasitoid ciliates. Science, 301, 339.Google Scholar
Gomez-Gutierrez, J., Strüder-Kypke, M.C., Lynn, D.H., Shaw, T.C., Aguilar-Méndez, M.J., López-Cortés, A. et al. 2012. Pseudocollinia brintoni gen. nov., sp. nov.(Apostomatida: Colliniidae), a parasitoid ciliate infecting the euphausiid Nyctiphanes simplex . Diseases of Aquatic Organisms, 99, 5778.Google Scholar
Hakariya, M., Hirose, D. & Tokumasa, S. 2009. Molecular phylogeny of terrestrial holocarpic endoparasititc peronosporomycetes, Haptoglossa spp., inferred from 18S rDNA. Mycoscience, 50, 130136.Google Scholar
Hamner, W.M. 1984. Aspects of schooling of Euphausia superba . Journal of Crustacean Biology, 4, 6774.Google Scholar
Iritani, D., Wakeman, K.C. & Leander, B.S. 2018. Molecular phylogenetic positions of two new marine gregarines (Apicomplexa)—Paralecudina anankea n. sp. and Lecudina caspera n. sp. from the intestine of Lumbrineris inflata (Polychaeta) show patterns of coevolution. Journal of Eukaryotic Microbiology, 65, 211219.Google Scholar
Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., et al. 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature, 454, 515518.Google Scholar
Lima-Mendez, G., Faust, K., Henry, N., Decelle, J., Colin, S., Carcillo, F., et al. 2015. Determinants of community structure in the global plankton interactome. Science, 348, 10.1126/science.1262073.Google Scholar
Lynn, D.H., Gómez-Gutiérrez, J., Strűder-Kypke, M.C. & Shaw, C.T. 2014. Ciliate species diversity and host-parasitoid codiversification in Pseudocollinia infecting krill, with description of Pseudocollinia similis sp. nov. Diseases of Aquatic Organisms, 112, 89102.Google Scholar
Mauchline, J. 1980. Measurements of body length of Euphausia superba Dana. BIOMASS Handbook No. 4, 9 pp.Google Scholar
Morgulis, A., Coulouris, G., Raytselis, Y., Madden, T.L., Agarwala, R. & Schäffer, A.A. 2008. Database indexing for production MegaBLAST searches. Bioinformatics, 24, 17571764.Google Scholar
Nicol, S. & Foster, J. 2016. The fishery for Antarctic krill: its current status and management regime. In Siegel, V., ed. Biology and ecology of Antarctic krill. Cham: Springer, 441 pp. 10.1007/978-3-319-29279-3_11.Google Scholar
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590D596.Google Scholar
Quetin, L.G. & Ross, R.M. 1991. Behavioural and physiological characteristics of the Antarctic krill, Euphausia superba . American Zoology, 31, 4963.Google Scholar
Rueckert, S. & Leander, B.S. 2008. Morphology and phylogenetic position of two novel marine gregarines (Apicomplexa, Eugregarinorida) from the intestines of North-eastern Pacific ascidians. Zoologica Scripta, 37, 637645.Google Scholar
Sameoto, D., Cochrane, N. & Herman, A. 1993. Convergence of acoustic, optical, and net-catch estimates of euphausiid abundance: use of artificial light to reduce net avoidance. Canadian Journal of Fisheries and Aquatic Sciences, 50, 334346.Google Scholar
Searle, C.L., Ochs, J.H., Cáceres, C.E., Chiang, S.L., Gerardo, N.M., Hall, S.R., et al . 2015. Plasticity, not genetic variation, drives infection success of a fungal parasite. Parasitology, 142, 839848.Google Scholar
Sokolova, M.N. 1994. Euphausiid ''dead body rain'' as a source of food for abyssal benthos. Deep-Sea Research I, 4, 741746.Google Scholar
Stankovic, A.M. & Rakusa-Suszczewski, S. 1996. Parasitic protozoa on appendages and inside the body of Euphausia superba Dana. Polish Polar Research, 17, 169171.Google Scholar
Suh, H.L. & Nemoto, T. 1988. Morphology of the gastric mill in ten species of euphausiids. Marine Biology, 97, 7985.Google Scholar
Takahashi, T.K., Kawaguchi, S., Kobayashi, M. & Toda, T. 2003. Parasitid eugregarines change their spatial distribution within the host digestive tract of Antarctic krill, Euphausia superba. Polar Biology, 26, 468473.Google Scholar
Takahashi, T.K., Kawaguchi, S., Kobayashi, M., Toda, T., Tanimura, A., Fukuchi, M., et al. 2011, Eugregarine infection within the digestive tract of larval Antarctic krill, Euphausia superba. Polar Biology, 34, 11671174.Google Scholar
Vidal, V., Ortiz, J., Diaz, J.I., Zafrilla, B., Bonete, M.J., De Ybanez, M.R., et al . 2016. Morphological, molecular and phylogenetic analyses of the spirurid nematode Stegophorus macronectes (Johnston & Mawson, 1942). Journal of Helminthology, 90, 214222.Google Scholar
Wallis, J.R., Smith, A.J.R. & Kawaguchi, S. 2017. Discovery of gregarine parasitism in some Southern Ocean krill (Euphausiacea) and the salp Salpa thompsoni . Polar Biology, 40, 19121917.Google Scholar
Wiebe, P.H., Ashijian, C.J., Gallager, S.M., Davis, C.S., Lawson, G.L. & Copley, N.L. 2004. Using a high-powered strobe light to increase the catch of Antarctic krill. Marine Biology, 144, 493502.Google Scholar
Wiebe, P.H., Morton, A.W., Bradley, A.M., Backus, A.M., Craddock, J.E., Barber, V., et al. 1985. New development in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Marine Biology, 87, 313323.Google Scholar