New records of deep-sea Gastrotricha and Tardigrada from Iberian and Canary Basins (Northeast Atlantic) with comments on abyssal meiofauna composition and the meiofauna paradox

Keywords: Atlantic Ocean, biodiversity, biogeography, deep sea, Desmodasys, Musellifer, Coronarctus

Abstract

The “meiofauna paradox” refers to the amphi-oceanic or even cosmopolitan distribution of species of this ecological group, i.e. the marine meiofauna, as opposed to their weak dispersal potential. Dissolving this paradox includes on the one hand the discovery of complexes of genetically distinct but morphological cryptic species with much more limited distribution areas, but also involves the investigation of “stepping stone habitats” like the shelf area of oceanic islands and summits of seamounts. Such biotopes subdivide long distances, e.g. from one continent to the other, into shorter sections. However, what needs to be excluded is a possible distribution of “shallow water meiofauna” simply via population growth and range expansion at the abyssal plains of the world's oceans. In order to test if the abyssal plains may represent a barrier against dispersal of certain marine meiofauna taxa, we studied the composition of the meiofauna from six samples (stations) taken during the expedition IceDivA (SO280) of the R/V Sonne to the Iberian and Canary Basins from abyssal depths (4904-5485 m). The taxonomic focus was put on the Gastrotricha and Tardigrada. The dominant taxa in all samples were nematodes (13.0 - 97.7 ind./cm2) and copepods (0.4 - 9.6 ind./cm2), followed by annelids, kinorhynchs and ostracods. Three Gastrotricha species (Desmodasys sp. iberianA, Desmodasys sp. langsethA, Musellifer sp. iberianA (Musellifer aff. tridentatus)) and one tardigrade (Coronarctus dissimilis) were registered and examined using light microscopy (DIC and CLSM) and SEM. All gastrotrichs from the examined samples presumably represent new and still undescribed species. The range of geographic and bathymetric distribution of Coronarctus dissimilis increases to the Iberian Basin and to a depth of 4163 m. This finding further hints to a potential amphi-Atlantic distribution of this species. We compare our data with those from other studies on seamounts, oceanic islands and from the deep-sea and conclude that the abyssal plains represent a significant barrier against long distance dispersal for most genera (and species) of Gastrotricha and for a certain fraction of genera of Tardigrada, too.

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Author Biographies

R. Trokhymchuk, V.N.Karazin Kharkiv National University

Svobody Maidan, 4, 61022, Kharkiv, Ukraine, rtrokhymchuk@gmail.com

A. Kieneke, German Centre for Marine Biodiversity Research (DZMB)

Senckenberg am Meer, Suedstrand 44, 26382, Wilhelmshaven, Germany, alexander.kieneke@senckenberg.de

References

Armonies, W., Reise, K. (2000). Faunal diversity across a sandy shore. Marine Ecology Progress Series 196, 49-57. https://doi.org/10.3354/meps196049

Bartels, P. J., Fontoura, P., Nelson, D. R. Kaczmarek, Ł. (2024). Intertidal and shallow subtidal marine tardigrades from the British Virgin Islands with a description of a new Batillipes (Heterotardigrada: Batillipedidae). Marine Biodiversity, 54(4), 60. https://doi.org/10.1007/s12526-024-01450-8

Boetius, A., Purser, A. (2017). The Expedition PS101 of the Research Vessel POLARSTERN to the Arctic Ocean in 2016. In Berichte zur Polar- und Meeresforschung = Reports on Polar and Marine Research (Vol. 706, pp. 1-230). Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung. https://doi.org/10.2312/BzPM_0706_2017

Bogorov, W. G. (1927). Zur Methodik der Bearbeitung des Planktons. (Eine neue Kammer zur Bearbeitung des Zooplanktons). Russian Hydrobiological Zhurnal, 6, 193-198.

Brix, S., Taylor, J., George, K. H., Tewes, S., Jenssen, C., Shipboard Scientific Party. (2024). Icelandic marine Animals: Genetics and Ecology meets Diversity along latitudinal gradients in the deep sea of the Atlantic Ocean, Cruise No. SO280, 08.01.2021 - 07.02.2021, Emden (Germany) - Emden (Germany). In SONNE-Berichte (SO280, pp. 1-36). Begutachtungspanel Forschungsschiffe. https://doi.org/10.48433/cr_so280

Bussau, C. (1992). New deep-sea Tardigrada (Arthrotardigrada, Halechiniscidae) from manganese nodule area of the eastern South Pacific. Zoologica Scripta, 21(1), 79-91. https://doi.org/10.1111/j.1463-6409.1992.tb00311.x

Clausen, C. (1965). Desmodasys phocoides gen., et sp. n., family Turbanellidae (Gastrotricha Macrodasyoidea). Sarsia, 21(1), 17-21. https://doi.org/10.1080/00364827.1965.10409557

Clausen, C. (2000). Gastrotricha Macrodasyida from the Tromsø region, northern Norway. Sarsia, 85(5-6), 357-384. https://doi.org/10.1080/00364827.2000.10414588

Cerca, J., Purschke, G., Struck, T. H. (2018). Marine connectivity dynamics: clarifying cosmopolitan distributions of marine interstitial invertebrates and the meiofauna paradox. Marine Biology, 165, 1-21. https://doi.org/10.1007/s00227-018-3383-2

Cerca, J., Meyer, C., Purschke, G., Struck, T. H. (2020). Delimitation of cryptic species drastically reduces the geographical ranges of marine interstitial ghost-worms (Stygocapitella; Annelida, Sedentaria). Molecular Phylogenetics and Evolution, 143, 106663.https://doi.org/10.1016/j.ympev.2019.106663

Derycke, S., Remerie, T., Backeljau, T., Vierstraete, A., Vanfleteren, J., Vincx, M., Moens, T. (2008). Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic. Molecular ecology, 17(14), 3306-3322. https://doi.org/10.1111/j.1365-294X.2008.03846.x

Dinet, A., Vivier, M. H. (1977). Le méiobenthos abyssal du Golfe de Gascogne I. Considérations sur les données quantitatives. Cahiers Biologie Marine, 18, 85-97.

Fattorini, S. (2017). Endemism in historical biogeography and conservation biology: concepts and implications. Biogeographia–The Journal of Integrative Biogeography, 32(1). https://doi.org/10.21426/B632136433

Fontaneto, D., Plewka, M. (2021). Phylum Rotifera. In Invertebrate Zoology (pp. 265-278). CRC Press.

Gąsiorek, P. (2023). Catch me if you can, or how paradigms of tardigrade biogeography evolved from cosmopolitism to ‘localism’. Zoological Journal of the Linnean Society, zlad191. https://doi.org/10.1093/zoolinnean/zlad191

George, K. H. (2013). Faunistic research on metazoan meiofauna from seamounts–a review. Meiofauna marina, 20(February), 1-32.

Giere, O. (2009). Meiofauna Taxa: A systematic account. Meiobenthology: the microscopic motile fauna of aquatic sediments, 103-234.

Hansen, J. G., Jørgensen, A., Kristensen, R. M. (2001). Preliminary studies of the tardigrade fauna of the Faroe Bank. Zoologischer Anzeiger-A Journal of Comparative Zoology, 240(3-4), 385-393. https://doi.org/10.1078/0044-5231-00046

Hansen, J.G., D'Addabbo Gallo, M. Grimaldi De Zio, S. (2003). A comparison of morphological characters within the genus Rhomboarctus (Tardigrada: Heterotardigrada) with the description of two new species. Zoologischer Anzeiger - A Journal of Comparative Zoology. 242(1), 83-96. https://doi.org/10.1078/0044-5231-00089

Hansen, J. G. (2007). The deep sea elements of the Faroe Bank tardigrade fauna with a description of two new species. J. Limnol, 66(1), 12-20. https://doi.org/10.4081/jlimnol.2007.s1.12

Hansen, J. G., Kristensen, R. M. Jørgensen, A. (2012). The armoured marine tardigrades (Arthrotardigrada, Tardigrada). Scientia Danica, series B Biologica 2, The Royal Danish Academy of Sciences and Letters, pp. 91.

Hansen, J. G., &Kristensen, R. M. (2021). A new genus and five new species of the subfamily Florarctinae (Tardigrada, Arthrotardigrada). European Journal of Taxonomy. 762, 149-184. https://doi.org/10.5852/ejt.2021.762.1461

Higgins, R. P., Thiel, H. (1988). Introduction to the study of meiofauna. Smithsonian Institution Press.

Hummon, W. D. (1969). Musellifer sublitoralis, a new genus and species of Gastrotricha from the San Juan Archipelago, Washington. Transactions of the American Microscopical Society, 88(2), 282-286. https://doi.org/10.2307/3224502

Hummon, W.D., ed. 2001-2010. Global Distribution of Marine Gastrotricha (at http://www.gastrotricha.unimore.it/checklist.htm)

Ingels, J., Valdes, Y., Pontes, L. P., Silva, A. C., Neres, P. F., Corrêa, G. V., ... dos Santos, G. A. (2020). Meiofauna life on loggerhead sea turtles-diversely structured abundance and biodiversity hotspots that challenge the meiofauna paradox. Diversity, 12(5), 203. https://doi.org/10.3390/d12050203

Jørgensen, A., Kristensen, R. M. (2001). A new tanarctid arthrotardigrade with buoyant bodies. Zoologischer Anzeiger-A Journal of Comparative Zoology, 240(3-4), 425-439. https://doi.org/10.1078/0044-5231-00051

Jørgensen, A., Boesgaard, T. M., Møbjerg, N. Kristensen, R. M. (2014) The tardigrade fauna of Australian marine caves: With descriptions of nine new species of Arthrotardigrada. Zootaxa, 3802(4), 401-433. https://doi.org/10.1078/0044-5231-00033

Jörger, K. M., Norenburg, J. L., Wilson, N. G., Schrödl, M. (2012). Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC evolutionary biology, 12, 1-18. https://doi.org/10.1186/1471-2148-12-245

Kaczmarek, Ł., Bartels, P. J., Roszkowska, M., Nelson, D. R. (2015). The zoogeography of marine Tardigrada. Zootaxa, 4037(1), 1-189. https://doi.org/10.11646/zootaxa.4037.1.1

Kånneby, T., Atherton, S., Hochberg, R. (2014). Two new species of Musellifer (Gastrotricha: Chaetonotida) from Florida and Tobago and the systematic placement of the genus within Paucitubulatina. Marine Biology Research, 10(10), 983-995. https://doi.org/10.1080/17451000.2013.872797

Kieneke, A. (2010). A new species of Thaumastoderma (Gastrotricha: Macrodasyida) from the Antarctic deep sea with a phylogenetic analysis of the whole genus. Journal of the Marine Biological Association of the United Kingdom, 90(3), 575-584. https://doi.org/10.1017/S002531540900085X

Kieneke, A., Zekely, J. (2008). Desmodasys abyssalis sp. nov.— first record of a deep-sea gastrotrich from hydrothermal vents. Marine Biodiversity Records, 1, e88. https://doi.org/10.1017/S1755267207008950

Kieneke, A., Münter, L. Riemann, O. (2020): Gastrotricha. In: Schmidt-Rhaesa, A. (ed.): Guide to the Identification of Marine Meiofauna, Verlag Dr. Friedrich Pfeil, München, pp. 104-163.

Kieneke, A. Brix, S. (2021). IceDivA (SO280) Eine Tiefseeexpedition zur Vernetzung langjähriger Messdaten und Proben (GfBS newsletter 39). 39, 16-23.

Kolicka, M. (2016). Gastrotrichs in bromeliads—newly recorded Chaetonotus (Hystricochaetonotus) furcatus Kisielewski, 1991 (Chaetonotida) from the Łódź Palm House. Zoosystema, 38(1), 141-155. https://doi.org/10.5252/z2016n1a5

Kreuzinger-Janik, B., Majdi, N., Traunspurger, W. (2021). Distribution and diversity of meiofauna along an aquatic-terrestrial moss ecotone. Nematology, 23(6), 695-714. https://doi.org/10.1163/15685411-bja10070

Kristensen, R. M., Renaud-Mornant, J. (1983). Existence d'Arthrotardigrades semi-benthiques de genres nouveaux de la sous-famille des Styraconyxinae subfam. nov. Cahiers de Biologie marine, 24, 337-353.

Kristensen, R. M., Sørensen, M. V., Hansen, J. G., Zeppilli, D. (2015). A new species of Neostygarctus (Arthrotardigrada) from the Condor Seamount in the Azores, Northeast Atlantic. Marine Biodiversity, 45, 453-467. https://doi.org/10.1007/s12526-015-0323-y

Leasi, F., Todaro, M. A. (2008). The muscular system of Musellifer delamarei (Renaud-Mornant, 1968) and other chaetonotidans with implications for the phylogeny and systematization of the Paucitubulatina (Gastrotricha). Biological Journal of the Linnean Society, 94(2), 379-398. https://doi.org/10.1111/j.1095-8312.2008.00974.x

Leasi, F., Todaro, M. A. (2010). The gastrotrich community of a north Adriatic Sea site, with a redescription of Musellifer profundus (Chaetonotida: Muselliferidae). Journal of the Marine Biological Association of the United Kingdom, 90(4), 645-653. https://doi.org/10.1017/S0025315409991068

Magpali, L., Machado, D. R., Araújo, T. Q., Garraffoni, A. R. (2021). Long distance dispersal and pseudo-cryptic species in Gastrotricha: first description of a new species (Chaetonotida, Chaetonotidae, Polymerurus) from an oceanic island with volcanic rocks. European journal of taxonomy, 746, 62-93. https://doi.org/10.5852/ejt.2021.746.1319

Martínez, A., Eckert, E.M., Artois, T.,Careddu, G., Casu,M., Curini-Galletti, M., Gazale, V., Gobert, S., Ivanenko , V.N., Jondelius, U., Marzano, M., Pesole, G., Zanello, A., M. Todaro, A., Fontaneto, D. (2020): Human access impacts biodiversity of microscopic animals in sandy beaches. Communications Biology 3, 175. https://doi.org/10.1038/s42003-020-0912-6

Minowa, A. K., Kieneke, A., Campos, A., Balsamo, M., Guidi, L., Araújo, T. Q. Garraffoni, A. R. S. New branch of the Tree of Life of Gastrotrich: Establishment of a new genus for limno-terrestrial species. Zoological Journal of the Linnean Society. (under revision)

Nelson, D. R., Guidetti, R., Rebecchi, L. (2015). Phylum tardigrada. In Thorp and Covich's Freshwater invertebrates (pp. 347-380). Academic Press.

Radziejewska, T., Gruzka, P., Rokicka-Praxmajer, J. (2006): A home away from home: a meiobenthic assemblage in a ship’s ballast water tank sediment. Oceanologia, 48, 259–265.

Ramirez-Llodra, E., Brandt, A., Danovaro, R., De Mol, B., Escobar, E., German, C. R., ... Vecchione, M. (2010). Deep, diverse and definitely different: unique attributes of the world's largest ecosystem. Biogeosciences, 7(9), 2851-2899. https://doi.org/10.5194/bg-7-2851-2010

Rao, G. C., Clausen, C. (1970). Planodasys marginalis gen. et sp. nov. and Planodasyidae fam. nov.(Gastotricha Magrodasyoidea). Sarsia, 42(1), 73-82. https://doi.org/10.1080/00364827.1970.10411164

Remane, A. (1925). Organisation und systematische Stellung der aberranten Gastrotrichen. Verhandlungen der deutschen zoologischen Gesellschaft, 30, 121-128.

Remane A. (1927). Beiträge zur Systematik der Süsswassergastrotrichen. Zoologische Jahrbücher. Abteilung für Systematik. 53(12), 269-320.

Remane, A. (1926). Morphologie und Verwandtschaftsbeziehungen der aberranten Gastrotrichen I. Zeitschrift für Morphologie und Ökologie der Tiere, 625-754.

Renaud-Mornant, J. (1968). Présence du genre Polymerurus en milieu marin, description de deux espèces nouvelles (Gastrotricha, Chaetonotoidae). Pubblicazioni della Stazione Zoologica di Napoli. 36,141 – 51.

Renaud-Mornant, J. (1988). Développement postembryonnaire du Tardigrade abyssal Coronarctus laubieri Renaud-Mornant, J. (1987) (Tardigrada, Heterotardigrada). Bulletin du Muséum national d'histoire naturelle. Section A, Zoologie, biologie et écologie animales, 10(2), 327-345. https://doi.org/10.5962/p.292211

Renaud-Mornant, J. (1987). Bathyal and abyssal Coronarctidae (Tardigrada), descriptions of new species and phylogenetical significance. In: R. Bertolani, editor. Biology of Tardigrades. Selected Symposia and Monographs U.Z.I., 1. Mucchi, Modena, Italy, 93–101.

Romano Iii, F., Gallo, M., D’Addabbo, R., Accogli, G., Baguley, J., Montagna, P. (2011). Deep-sea tardigrades in the northern Gulf of Mexico with a description of a new species of Coronarctidae (Tardigrada: Arthrotardigrada), Coronarctus mexicus. Journal of Zoological Systematics and Evolutionary Research, 49, 48-52. https://doi.org/10.1111/j.1439-0469.2010.00597.x

Santos, E., Veiga, P., Rubal, M., Bartels, P. J., da Rocha, C. M. Fontoura, P. (2019). Batillipes pennaki Marcus, 1946 (Arthrotardigrada: Batillipedidae): deciphering a species complex. Zootaxa, 4648(3), zootaxa-4648. https://doi.org/10.11646/zootaxa.4648.3.9

Sergeeva, N., Ürkmez, D., Todaro, M. A. (2019). Significant occurrence of Musellifer profundus Vivier, 1974 (Gastrotricha, Chaetonotida) in the Black Sea. Check List, 15(1), 219-224. https://doi.org/10.15560/15.1.219

Shimabukuro, M., Zeppilli, D., Leduc, D., Wenzhöfer, F., Berg, P., Rowden, A. A., Glud, R. N. (2022). Intra-and inter-spatial variability of meiofauna in hadal trenches is linked to microbial activity and food availability. Scientific reports, 12(1), 4338. https://doi.org/10.1038/s41598-022-08088-1

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676–682. https://doi.org/10.1038/nmeth.2019

Thiel, H. (1975). The size structure of the deep-sea benthos. Integrationale Revevue der gesamten Hydrobiologie. 60, 575–606

Todaro, M. A. D., Hummon, W. D. (2008). An overview and a dichotomous key to genera of the phylum Gastrotricha. Meiofauna Marina, 16, 3-20.

Traunspurger, W., Majdi, N. (2017). Meiofauna. In: Methods in Stream Ecology, Volume 1 (pp. 273-295). Academic Press.

Trokhymchuk, R., Kieneke, A. (2024). Novel distribution records of marine Tardigrada from abyssal sediments of the Northwest Atlantic Ocean. Organisms Diversity & Evolution, 1-16. https://doi.org/10.1007/s13127-024-00641-2

Trokhymchuk, R., Schmidt-Rhaesa, A., Utevsky, S., Kristensen, R. M., Kieneke, A. (2024) Towards a better understanding of deep-sea tardigrade biogeography: numerous new records and a new species from the Southern Ocean. Zootaxa, 5543(1), 1-39. https://doi.org/10.11646/zootaxa.5543.1.1

Tchesunov, A. V. (2018). A new tardigrade species of the genus Neostygarctus Grimaldi de Zio et al., 1982 (Tardigrada, Arthrotardigrada) from the Great Meteor Seamount, Northeast Atlantic. European Journal of Taxonomy, (479). https://doi.org/10.5852/ejt.2018.479

Vincx, M., Bett, B. J., Dinet, A., Ferrero, T., Gooday, A. J., Lambshead, P. J. D., ... Vanreusel, A. (1994). Meiobenthos of the deep Northeast Atlantic. In: Advances in Marine Biology (Vol. 30, pp. 1-88). Academic Press. https://doi.org/10.1016/S0065-2881(08)60061-9

Westheide, W., Haß-Cordes, E., Krabusch, M., Müller, M. (2003). Ctenodrilus serratus (Polychaeta: Ctenodrilidae) is a truly amphi-Atlantic meiofauna species–evidence from molecular data. Marine Biology, 142, 637-642. https://doi.org/10.1007/s00227-002-0960-0

Zeppilli, D., Bongiorni, L., Cattaneo, A., Danovaro, R., Santos, R. S. (2013). Meiofauna assemblages of the Condor Seamount (North-East Atlantic Ocean) and adjacent deep-sea sediments. Deep Sea Research Part II: Topical Studies in Oceanography, 98, 87-100 https://doi.org/10.1016/j.dsr2.2013.08.009.

Published
2024-12-23
Cited
How to Cite
Trokhymchuk, R., & Kieneke, A. (2024). New records of deep-sea Gastrotricha and Tardigrada from Iberian and Canary Basins (Northeast Atlantic) with comments on abyssal meiofauna composition and the meiofauna paradox. The Journal of V.N.Karazin Kharkiv National University. Series «Biology», 43, 66-84. https://doi.org/10.26565/2075-5457-2024-43-6
Section
ZOOLOGY AND ECOLOGY