Extremely high abundances of Prasiola crispa-associated micrometazoans in East Antarctica

  • Dzmitry A. Lukashanets Marine Research Institute, Klaipėda University, Klaipėda, Lithuania; and Institute of Oceanology, Polish Academy of Sciences, Sopot, Poland
  • Yury H. Hihiniak State Scientific and Practical Center for Bioresources, National Academy of Sciences of Belarus, Minsk, Belarus
  • Vladislav Y. Miamin State Scientific and Practical Center for Bioresources, National Academy of Sciences of Belarus, Minsk, Belarus; and Biology Faculty, Belarusian State University, Minsk, Belarus
Keywords: Bdelloids, rotifers, tardigrades, algae, nematodes, Antarctic oases

Abstract

To elucidate poorly known aspects of the microscopic metazoan distribution in ice-free parts of the Antarctic, we examined samples of the multicellular terrestrial alga Prasiola crispa, collected over the last decade in different parts of continental East Antarctica and Haswell Island. We found that the micrometazoans inhabiting the algae consist of remarkably abundant bdelloid rotifers (subclass Bdelloidea), followed by tardigrades. We did not find nematodes. The rotifer assemblages were characterized by low diversity (only six species). Nevertheless, rotifer densities were extremely high: mean densities ranged from 75 to 3030 individuals per 100 mg of the dry sample weight and the maximum value numbered in excess of 8000 per 100 mg of the dry sample weight. These data show that terrestrial algae, along with mosses, are a very attractive habitat for rotifers and tardigrades in the Antarctic. The statistical analysis showed a lack of correlations between rotifer and tardigrade densities and nutrients (N, C, P, K and Na). Our findings are consistent with the patchy distribution of terrestrial micrometazoans in the Antarctic that has previously been found.

Downloads

Download data is not yet available.

References


Adams B.J., Bardgett R.D., Ayres E., Wall D.H., Aislabie J., Bamforth S., Bargagli R., Cary C., Cavacini P., Connell L., Convey P., Fell J.W., Frati F., Hogg I.D., Newsham K.K., O’Donnell A., Russell N., Seppelt R.D. & Stevens M.I. 2006. Diversity and distribution of Victoria Land biota. Soil Biology and Biochemistry 38, Spec. Issue S1, 3003–3018, doi: 10.1016/j.soilbio.2006.04.030.


Almela P., Velázquez D., Rico E., Justel A. & Quesada A. 2019. Carbon pathways through the food web of a microbial mat from Byers Peninsula, Antarctica. Frontiers in Microbiology 10, article no. 628, doi: 10.3389/fmicb.2019.00628.


Andriuzzi W.F., Adams B.J., Barrett J.E., Virginia R.A. & Wall D.H. 2018. Observed trends of soil fauna in the Antarctic Dry Valleys: early signs of shifts predicted under climate change. Ecology 99, 312–321, doi: 10.1002/ecy.2090.


Bingemer J. & Hohberg K. 2017. An illustrated identification key to the Eutardigrade species (Tardigrada, Eutardigrada) presently known from European soils. Soil Organisms 89, 127–149.


Block W., Lewis Smith R.I. & Kennedy A.D. 2009. Strategies of survival and resource exploitation in the Antarctic fellfield ecosystem. Biological Reviews 84, 449–484, doi: 10.1111/j.1469-185X.2009.00084.x.


Bokhorst S., Convey P. & Aerts R. 2019. Nitrogen inputs by marine vertebrates drive abundance and richness in Antarctic terrestrial ecosystems. Current Biology 29, 1721–1727, doi: 10.1016/j.cub.2019.04.038.


Bokhorst S., Ronfort C., Huiskes A., Convey P. & Aerts R. 2007. Food choice of Antarctic soil arthropods clarified by stable isotope signatures. Polar Biology 30, 983–990, doi: 10.1007/s00300-007-0256-4.


Caruso T., Hogg I.D., Nielsen U.N., Bottos E.M., Lee C.K., Hopkins D.W., Cary S.C., Barrett J.E., Green T.G.A., Storey B.C., All D.H. & Adams B.J. 2019. Nematodes in a polar desert reveal the relative role of biotic interactions in the coexistence of soil animals. Communications Biology 2, article no. 63, doi: 10.1038/s42003-018-0260-y.


Chown S.L., Lee J.E., Hughes K.A., Barnes J., Barrett P.J., Bergstrom D.M., Convey P., Cowan D.A., Crosbie K., Dyer G., Frenot Y., Grant S.M., Herr D., Kennicutt M.C. II, Lamers M., Murray A., Possingham H.P., Reid K., Riddle M.J., Ryan P.G., Sanson L., Shaw J.D., Sparrow M.D., Summerhayes C., Terauds A. & Wall D.H. 2012. Challenges to the future conservation of the Antarctic. Science 337, 158–159, doi: 10.1126/science.1222821.


Convey P. 1996. Overwintering strategies of terrestrial invertebrates in Antarctica—the significance of flexibility in extremely seasonal environments. European Journal of Entomology 93, 489–505.


Convey P. 2010. Terrestrial biodiversity in Antarctica—recent advantages and future challenges. Polar Science 4, 135–147, doi: 10.1016/j.polar.2010.03.003.


Convey P., Biersma E.M., Casanova-Katny A. & Maturana C.S. 2020. Refuges of Antarctic diversity. In M. Oliva & J. Ruiz-Fernández (eds.): Past Antarctica. Pp. 181–200. Burlington: Academic Press.


Convey P., Chown S.L., Clarke A., Barnes D.K.A., Bokhorst S., Cummings V., Ducklow H.W., Frati F., Green T.G.A., Gordeon S., Griffiths H.J., Howard-Williams C., Huiskes A.H.L., Laybourn-Parry J., Lyons W.B., McMinn A., Morley S.A., Peck L.S., Guesada A., Robinson S.A., Schiaparelli S. & Wall D.H. 2014. The spatial structure of Antarctic biodiversity. Ecological Monographs 84, 203–244, doi: 10.1890/12-2216.1.


Convey P., Gibson J., Hillenbrand C.D., Hodgson D.A., Pugh P J.A., Smellie J.L. & Stevens M.I. 2008. Antarctic terrestrial life—challenging the history of the frozen continent? Biological Reviews of the Cambridge Philosophical Society 83, 103–117, doi: 10.1111/j.1469-185X.2008.00034.x.


Convey P. & McInnes S.J. 2005. Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica. Ecology 86, 519–527, doi: 10.1890/04-0684.


Convey P. & Peck L.S. 2019. Antarctic environmental change and biological responses. Science Advances 11, eaaz0888, doi: 10.1126/sciadv.aaz0888.


Convey P. & Stevens M.I. 2007. Antarctic biodiversity. Science 317, 1877–1878, doi: 10.1126/science.1147261.


Dalto A.G., de Faria G.M., de Alencar Imbassahy C.A., de Souza Campos T.M. & Yoneshigue-Valentin Y. 2010. Associated fauna of Prasiola crispa (Chlorophyta) related to penguin rookery at Arctowski (King George Island, South Shetland Islands, maritime Antarctic). INCT-APA Annual Activity Report 2010, Thematic Area 3, 188–193, doi: 10.4322/apa.2014.048.


De Mendonça M.C., Queiroz G.C., Abrantes E.A., Dalto A.G. & Yoneshigue-Valentin Y. 2012. Collembola (Arthropoda, Hexapoda) associated to terrestrial green algae from ice-free areas in Admiralty Bay (King George Island, South Shetlands islands, Antarctica). Annual Activity Report. Science Highlights 2012, Thematic Area 2, 94–97, doi: 10.4322/apa.2014.103.


Donner J. 1965. Ordnung Bdelloidea (Rotatoria, Rädertiere). Bestimmungsbücher zur Bodenfauna Europas. (Order Bdelloidea [Rotatoria, rotifers]. Identification books on the soil fauna of Europe.) Berlin: Akademie.


Dougherty E.C. & Harris L.G. 1963. Antarctic Micrometazoa: fresh-water species in the McMurdo Sound Area. Science 140, 497–498, doi: 10.1126/science.140.3566.497.


Everitt D.A. 1981. An ecological study of an Antarctic freshwater pool with particular reference to Tardigrada and Rotifera. Hydrobiologia 83, 225–237, doi: 10.1007/BF00008270.


Fontaneto D., Iakovenko N. & De Smet W.H. 2015. Diversity gradients of rotifer species richness in Antarctica. Hydrobiologia 761, 235–248, doi: 10.1007/s10750-015-2258-5.


Fraser C.I., Nikula R., Ruzzante D.E. & Waters J.M. 2012. Poleward bound: biological impacts of Southern Hemisphere glaciation. Trends in Ecology & Evolution 27, 462–471, doi: 10.1016/j.tree.2012.04.011.


Gantz J.D., Spacht D.E. & Lee R.E. 2018. A preliminary survey of the terrestrial arthropods of the Rosenthal Islands, Antarctica. Polar Research 36, article no. 1500266, doi: 10.1080/17518369.2018.1500266.


Garlasché G., Karim K., Iakovenko N., Velasco-Castrillón A., Janko K., Guidetti R., Rebecchi L., Cecchetto M., Schiaparelli S., Jersabek C., De Smet W.H. & Fontaneto D. 2020. A data set on the distribution of Rotifera in Antarctica. Biogeographia—The Journal of Integrative Biogeography 35, 17–25, doi: 10.21426/B635044786.


Heatwole H. & Miller W.R. 2019. Structure of micrometazoan assemblages in the Larsemann Hills, Antarctica. Polar Biology 42, 1837–1848, doi: 10.1007/s00300-019-02557-6.


Iakovenko N.S., Kašparová E., Plewka M. & Janko K. 2013. Otostephanos (Rotifera, Bdelloidea, Habrotrochidae) with the description of two new species. Systematics and Biodiversity 24, 477–494, doi: 10.1080/14772000.2013.857737.


Iakovenko N.S., Smykla J., Convey P., Kašparová E., Kozeretska I.A., Trokhymets V., Dykyy I., Plewka M., Devetter M., Duris Z. & Janko K. 2015. Antarctic bdelloid rotifers: diversity, endemism and evolution. Hydrobiologia 761, 5–43, doi: 10.1007/s10750-015-2463-2.


Janetschek H. 1963. On the terrestrial fauna of the Ross Sea area, Antarctica. Pacific Insects 5, 305–311.


Janetschek H. 1967. Arthropod ecology of South Victoria Land. Entomology Antarctica 10, 205–293, doi: 10.1029/AR010p0205.


Jennings P.G. 1976. The Tardigrada of Signy Island, South Orkney Islands, with a note on the Rotifera. British Antarctic Survey Bulletin 44, 1–25.


Kutikova L.A. 2005. Bdelloidnye kolovratki fauny Rossii. (Bdelloid rotifers in fauna of Russia.) Moscow: The Community of Scientific Publications KMK.


Miller J.D., Horne P., Heatwole H., Miller W.R. & Bridges L. 1988. A survey of the terrestrial Tardigrada of the Vestfold Hills, Antarctica. Hydrobiologia 165, 197–208, doi: 10.1007/BF00025588.


Miller W.R. & Heatwole H. 1996. Tardigrades of the Australian Antarctic territories: the Windmill Islands, East Antarctica. Zoological Journal of the Linnaean Society 116, 175–184, doi: 10.1111/j.1096-3642.1996.tb02342.x.


Miller W.R., Heatwole H., Pidgeon R.W.J. & Gardiner G.R. 1994. Tardigrades of the Australian Antarctic Territories: the Larsemann Hills, East Antarctica. Transactions of the American Microscopical Society 113, 142–160, doi: 10.2307/3226642.


Miller W.R., Miller J.D. & Heatwole H. 1994. Tardigrades of the Australian Antarctic Territory: assessing diversity within a sample. Memoirs of the Queensland Museum 36, 137–145.


Murray J. 1910a. Antarctic Rotifera. British Antarctic Expedition 1907–1909. Reports of the Scientific Investigations, Biology 1(3), 41–73.


Murray J. 1910b. Microscopic life at Cape Royds. British Antarctic Expedition 1907–1909. Reports of the Scientific Investigations, Biology 1(2), 17–22.


Örstan A. 2020. The trouble with Adineta vaga (Davis, 1873): a common rotifer that cannot be identified (Rotifera: Bdelloidea: Adinetidae). Zootaxa 4830, 597–600, doi: 10.11646/zootaxa.4830.3.8.


Peters U., Koste W. & Westheide W. 1993. A quantitative method to extract moss-dwelling rotifers. Hydrobiologia 255/256, 339–341, doi: 10.1007/BF00025857.


Pilato G. & Binda M.G. 2010. Definition of families, subfamilies, genera and subgenera of the Eutardigrada, and keys to their identification. Zootaxa 2404, 1–54, doi: 10.11646/zootaxa.2404.1.1.


Poinar G. 2015. Phylum Nemata. In J.H. Thorp & D.C. Rogers (eds.): Thorp and Covich’s freshwater invertebrates. 4th edn. Pp. 273–302. Cambridge, UK: Academic Press.


Porazinska D.L., Fountain A.G., Nylen T.H., Tranter M., Virginia R.A. & Wall D.H. 2004. The biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arctic, Antarctic, and Alpine Research 36, 84–115, doi: 10.1657/1523-0430(2004)036[0084:TBABOC]2.0.CO;2.


Porazińska D.L., Wall D.H. & Virginia R.A. 2002a. Invertebrates in ornithogenic soils on Ross Island, Antarctica. Polar Biology 25, 569–574, doi: 10.1007/s00300-002-0386-7.


Porazińska D.L., Wall D.H. & Virginia R.A. 2002b. Population age structure of nematodes in the Antarctic Dry Valleys: perspectives on time, space, and habitat suitability. Arctic, Antarctic, and Alpine Research 34, 159–168, doi: 10.2307/1552467.


Pugh P.J.A. & Convey P. 2008. Surviving out in the cold: Antarctic endemic invertebrates and their refugia. Journal of Biogeography 35, 2176–2186, doi: 10.1111/j.1365-2699.2008.01953.x.


Ramazzotti G. & Maucci W. 1983. Phylum Tardigrada. Memorie dell’Istituto Italiano di Idrobiologia 41, 1–1012.


Rogers A.D., Johnston N.M., Murphy E.J. & Clarke A. 2012. Antarctic ecosystems: an extreme environment in a changing world. Oxford: Wiley-Blackwell.


Schulte G., Elnitsky M., Benoit J., Denlinger D. & Lee R. 2008. Extremely large aggregations of collembolan eggs on Humble Island, Antarctica: a response to early seasonal warming? Polar Biology 31, 889–892, doi: 10.1007/s00300-008-0445-9.


Segers H. 2007. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564, 1–104, doi: 10.11646/zootaxa.1564.1.1.


Shaw E.A., Adams B.J., Barrett J.E., Lyons W.B., Virginia R.A. & Wall D.H. 2018. Stable C and N isotope ratios reveal soil food web structure and identify the nematode Eudorylaimus antarcticus as an omnivore-predator in Taylor Valley, Antarctica. Polar Biology 41, 1013–1018, doi: 10.1007/s00300-017-2243-8.


Sinclair B.J., Scott M.B., Jaco Klok C., Terblanche J.S., Marshall D.J., Reyers B. & Chown S.L. 2006. Determinants of terrestrial arthropod community composition at Cape Hallett, Antarctica. Antarctic Science 18, 303–312, doi: 10.1017/S0954102006000356.


Sinclair B.J. & Sjursen H. 2001. Terrestrial invertebrate abundance across a habitat transect in Keble Valley, Ross Island, Antarctica. Pedobiologia 45, 134–145, doi: 10.1078/0031-4056-00075.


Smykla J., Iakovenko N., Devetter M. & Kaczmarek L. 2012. Diversity and distribution of tardigrades in soils of Edmonson Point (northern Victoria Land, continental Antarctica). Czech Polar Reports 2, 61–70, doi: 10.5817/CPR2012-2-6.


Smykla J., Porazinska D., Iakovenko N., Devetter M., Drewnik M., Hii Y. & Emslie S. 2018. Geochemical and biotic factors influencing the diversity and distribution of soil microfauna across ice-free coastal habitats in Victoria Land, Antarctica. Soil Biology and Biochemistry 116, 265–276, doi: 10.1016/j.soilbio.2017.10.028.


Smykla J., Porazinskia D.L., Iakovenko N., Janko K., Weiner W.M., Niedbala W. & Drewnik M. 2010. Studies on Antarctic soil invertebrates: preliminary data on rotifers (Rotatoria), with notes on other taxa from Edmonson Point (northern Victoria Land, continental Antarctic). Acta Societatis Zoologicae Bohemicae 74, 135–140.


Sohlenius B. & Boström S. 2005. The geographic distribution of metazoan microfauna on East Antarctic nunataks. Polar Biology 28, 439–448, doi: 10.1007/s00300-004-0708-z.


Sohlenius B. & Boström S. 2008. Species diversity and random distribution of microfauna in extremely isolated habitable patches on Antarctic nunataks. Polar Biology 31, 817–825, doi: 10.1007/s00300-008-0420-5.


Sohlenius B., Boström S. & Hirschfelder A. 1995. Nematodes, rotifers and tardigrades from nunataks in Dronning Maud Land, East Antarctica. Polar Biology 15, 51–56, doi: 10.1007/BF00236124.


Sohlenius B., Boström S. & Hirschfelder A. 1996. Distribution patterns of microfauna (nematodes, rotifers and tardigrades) on nunataks in Dronning Maud Land, East Antarctica. Polar Biology 16, 191–200, doi: 10.1007/BF02329207.


Sohlenius B., Boström S. & Jönsson K.I. 2004. Occurrence of nematodes, tardigrades and rotifers on ice-free areas in East Antarctica. Pedobiologia 48, 395–408, doi: 10.1016/j.pedobi.2004.06.001.


Sugg P., Edwards J.S. & Baust J. 1983. Phenology and life history of Belgica antarctica, an Antarctic midge (Diptera: Chironomidae). Ecological Entomology 8, 105–113, doi: 10.1111/j.1365-2311.1983.tb00487.x.


Suren A. 1990. Microfauna associated with algal mats in meltwater ponds of the Ross Ice Shelf. Polar Biology 10, 329–335, doi: 10.1007/BF00237819.


van den Hoogen J., Geisen S., Routh D., Ferris H., Traunspurger W., Wardle D.A., de Goede R.G.M., Adams B.J., Ahmad W., Andriuzzi W.S., Bardgett R.D., Bonkoswki M., Campos-Herrera R., Cares J.E., Caruso T., Caixeta L.D., Chen X.Y., Costa S.R., Creamer R., Castro J.M.D., Dam M., Djigal D., Escuer M., Griffiths B.S., Gutierrez C., Hohberg K., Kalinkina D., Kardol P., Kergenteuil A., Korthals G., Krashevska V., Kudrin A.A., Li Q., Liang W.J., Magilton M., Marais M., Martin J.A.R., Matveeva E., Mayad E., Mulder C., Mullin P., Neilson R., Nguyen T.A.D., Nielsen U.N., Okada H., Rius J.E.P., Pan K., Peneva V., Pellissier L., da Silva J.C.P., Pitteloud C., Powers T.O., Powers K., Quist C.W., Rasmann S., Moreno S.S., Scheu S., Setala H., Sushchuk A., Tiunov A.V., Trap J., van der Putten W., Vestergard M., Villenave C., Waeyenberge L., Wall D.H., Wilschut R., Wright D.G., Yang J.I. & Crowther T.W. 2019. Soil nematode abundance and functional group composition at a global scale. Nature 572, 194–198, doi: 10.1038/s41586-019-1418-6.


Velasco-Castrillón A., Gibson J.A.E. & Stevens M.I. 2014. A review of current Antarctic limno-terrestrial microfauna. Polar Biology 37, 1517–1531, doi: 10.1007/s00300-014-1544-4.


Velasco-Castrillón A., Hawes I. & Stevens M. 2018. 100 years on: a re-evaluation of the first discovery of microfauna from Ross Island, Antarctica. Antarctic Science 30, 209–219, doi: 10.1017/S095410201800007X.


Velasco-Castrillón A., McInnes S., Schultz M., Arróniz-Crespo M., D’Haese C., Gibson J., Adams B., Page T., Austin A., Cooper S. & Stevens M. 2015. Mitochondrial DNA analyses reveal widespread tardigrade diversity in Antarctica. Invertebrate Systematics 29, 578–590, doi: 10.1071/IS14019.


Velasco-Castrillón A., Page T.J., Gibson J.A.E. & Stevens M. 2014. Surprisingly high levels of biodiversity and endemism amongst Antarctic rotifers uncovered with mitochondrial DNA. Biodiversity 15, 130–142, doi: 10.1080/14888386.2014.930717.


Velasco-Castrillón A., Schultz M.B., Colombo F., Gibson J.A.E., Davies K.A., Austin A.D. & Stevens M.I. 2014. Distribution and diversity of soil microfauna from East Antarctica: assessing the link between biotic and abiotic factors. PLoS One 9, e87529, doi: 10.1371/journal.pone.0087529.


Velasco-Castrillón A. & Stevens M.I. 2014. Morphological and molecular diversity at a regional scale: a step closer to understanding Antarctic nematode biogeography. Soil Biology and Biochemistry 70, 272–284, doi: 10.1016/j.soilbio.2013.12.016.


Velázquez D., Jungblut A., Rochera C., Rico E., Camacho A. & Quesada A. 2017. Trophic interactions in microbial mats on Byers Peninsula, maritime Antarctica. Polar Biology 40, 1115–1126, doi: 10.1007/s00300-016-2039-2.


Wall D.H., Adams B.J., Barrett J.E., Hopkins D.W. & Virginia R.A. 2006. A synthesis of soil biodiversity and ecosystem functioning in Victoria Land, Antarctica. Soil Biology and Biochemistry 38, 3001–3002, doi: 10.1016/j.soilbio.2006.04.018.


Zawierucha K., Marshall C.J., Wharton D. & Janko K. 2019. A nematode in the mist: Scottnema lindsayae is the only soil metazoan in remote Antarctic deserts, at greater densities with altitude. Polar Research 38, article no. 3494, doi: 10.33265/polar.v38.3494.


Zawierucha K., Porazinska D.L., Ficetola G.F., Ambrosini R., Baccalo G., Buda J., Ceballos J.L., Devetter M., Dial R., Franzetti, Fuglewicz U., Gielly L., Lokas E., Janko K., Jaromerska T.N., Koscinski A., Kozlowska A., Ono M., Parnikoza I., Pittino F., Poniecka E., Sommers P., Schmidt S.K., Shain D., Sikorska S., Uetake J. & Takeuchi N. 2021. A hole in the nematosphere: tardigrades and rotifers dominate the cryoconite hole environment, whereas nematodes are missing. Journal of Zoology 313, 18–36, doi: 10.1111/jzo.12832.


Zawierucha K., Zmudczyńska-Skarbek K., Kaczmarek Ł. & Wojczulanis-Jakubas K. 2016. The influence of a seabird colony on abundance and species composition of water bears (Tardigrada) in Hornsund (Spitsbergen, Arctic). Polar Biology 39, 713–723, doi: 10.1007/s00300-015-1827-4.


Zmudczyńska K., Olejniczak I., Zwolicki A., Iliszko L., Convey P. & Stempniewicz L. 2012. Influence of allochtonous nutrients delivered by colonial seabirds on soil collembolan communities on Spitsbergen. Polar Biology 35, 1233–1245, doi: 10.1007/s00300-012-1169-4.


Zmudczyńska-Skarbek K., Barcikowski M., Drobniak S.M., Gwiazdowicz D.J., Richard P., Skubała P. & Stempniewicz L. 2017. Transfer of ornithogenic influence through different trophic levels of the Arctic terrestrial ecosystem of Bjørnøya (Bear Island), Svalbard. Soil Biology & Biochemistry 115, 475–489, doi: 10.1016/j.soilbio.2017.09.008.


Zmudczyńska-Skarbek K., Zwolicki A., Convey P., Barcikowski M. & Stempniewicz L. 2015. Is ornithogenic fertilization important for collembolan communities in Arctic terrestrial ecosystems? Polar Research 34, article no. 25629, doi: 10.3402/polar.v34.25629.
Published
2022-06-20
How to Cite
Lukashanets D. A., Hihiniak Y. H., & Miamin V. Y. (2022). Extremely high abundances of Prasiola crispa-associated micrometazoans in East Antarctica. Polar Research, 41. https://doi.org/10.33265/polar.v41.7781
Section
Research Articles