Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-29T07:19:41.170Z Has data issue: false hasContentIssue false

The first report of a parasitic ‘turbellarian’ from a cephalopod mollusc, with description of Octopoxenus antarcticus gen. nov., sp. nov. (Platyhelminthes: Fecampiida: Notenteridae)

Published online by Cambridge University Press:  17 October 2022

I. Gordeev*
Affiliation:
Russian Federal Research Institute of Fisheries and Oceanography, Moscow, Russia Lomonosov Moscow State University, Moscow, Russia
N. Biserova
Affiliation:
Lomonosov Moscow State University, Moscow, Russia
K. Zhukova
Affiliation:
Lomonosov Moscow State University, Moscow, Russia
I. Ekimova
Affiliation:
Lomonosov Moscow State University, Moscow, Russia
*
Author for correspondence: I. Gordeev, E-mail: gordeev_ilya@bk.ru

Abstract

Parasitic ‘turbellarians’ are known from various animals such as echinoderms, crustaceans, annelids, bivalve and gastropod molluscs. So far, however, no ‘turbellarians’ have been reported from cephalopods. In this paper we report a parasitic ‘turbellarian’ from the giant Antarctic octopus, Megaleledone setebos. We dissected two specimens of M. setebos caught in the Ross Sea (Antarctica) and found numerous worms in their intestine and liver. The worms were spherical or oblong and had two morphologically different poles. The frontal pole bears a small conical protrusion containing large elongated pear-shaped frontal glands and large polygonal cells. The ducts of the frontal glands open terminally to form the frontal organ. The caudal pole has an opening shaped as a folded tube connected by the genital pore with a common genital atrium, which continues into a canal with a muscular sheath. The worms were identified as ‘turbellarians’ from the family Notenteridae (Fecampiida). This family contains only one species, Notentera ivanovi, reported from the gut of a polychaete at the White Sea. The worms that we found in the gastrointestinal tract of the octopuses were morphologically similar to N. ivanovi but differed from it in several important respects. Phylogenetic analysis based on 28S rDNA gene showed that the newly found worm clustered together with other fecampiids in a highly supported clade and was closely related to N. ivanovi. On the basis of these morphological and molecular data, we described a new species, Octopoxenus antarcticus gen. nov., sp. nov. (Fecampiida: Notenteridae), establishing a new genus to accommodate it and provided an updated diagnosis of the family Notenteridae. This is the first report of a parasitic ‘turbellarian’ from a cephalopod mollusc.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215(3), 403410.CrossRefGoogle ScholarPubMed
Bacon, PJ, Dallas, JF and Piertney, SB (1999) Phylogeny of the Platyhelminthes and the evolution of parasitism. Biological Journal of the Linnean Society 68(1–2), 257287.Google Scholar
Bahia, J, Padula, V and Schrödl, M (2017) Polycladida phylogeny and evolution: integrating evidence from 28S rDNA and morphology. Organisms Diversity & Evolution 17(1), 653678.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83, 575583.Google Scholar
Byhovskaja-Pavlovskaja, IE (1985) Parasites of fishes: manual. 121 pp. Leningrad, Nauka.CrossRefGoogle Scholar
Cannon, LRG and Francis, S (1986) Turbellaria of the world: a guide to families and genera. 136 pp. South Brisbane, Queensland, Queensland Museum.Google Scholar
Chaban, EM, Ekimova, IA, Schepetov, DM and Chernyshev, AV (2019) Meloscaphander grandis (Heterobranchia: Cephalaspidea), a deep-water species from the North Pacific: Redescription and taxonomic remarks. Zootaxa 4646(2), 385400.Google ScholarPubMed
Christensen, AM (1981) The geographical and bathymetrical distribution of the Fecampiidae (Turbellaria, Rhabdocoela). Hydrobiologia 84(1), 1316.CrossRefGoogle Scholar
Curini-Galletti, M, Webster, BL, Huyse, T, Casu, M, Schockaert, ER, Artois, T and Littlewood, DTJ (2010) New insights on the phylogenetic relationships of the Proseriata (Platyhelminthes), with proposal of a new genus of the family Coelogynoporidae. Zootaxa 2537(1), 118.CrossRefGoogle Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5), 17921797.Google ScholarPubMed
Egger, B, Lapraz, F, Tomiczek, B, et al. (2015) A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Current Biology 25(10), 13471353.CrossRefGoogle ScholarPubMed
Hochberg, FG (1982) The ‘kidneys’ of cephalopods: a unique habitat for parasites. Malacologia 23(1), 121134.Google Scholar
Hyra, GS (1993) Genostoma kozloffi sp. nov. and G. inopinatum sp. nov. (Turbellaria: Neorhabdocoela: Genostomatidae) from leptostracan crustaceans of the genus Nebalia. Cahiers de Biologie Marine 34(1), 111126.Google Scholar
Janssen, T, Vizoso, DB, Schulte, G, Littlewood, DTJ, Waeschenbach, A and Schärer, L (2015) The first multi-gene phylogeny of the Macrostomorpha sheds light on the evolution of sexual and asexual reproduction in basal Platyhelminthes. Molecular Phylogenetics and Evolution 92(1), 82107.Google ScholarPubMed
Jennings, JB (1971) Parasitism and commensalism in the Turbellaria. Advances in Parasitology 9(1), 132.CrossRefGoogle Scholar
Jennings, JB (1989) Epidermal uptake of nutrients in an unusual turbellarian parasitic in the starfish Coscinasterias calamaria in Tasmanian waters. Biology Bulletin 176(3), 327336.CrossRefGoogle Scholar
Jennings, JB (1997) Nutritional and respiratory pathways to parasitism exemplified in the Turbellaria. International Journal for Parasitology 27(6), 679691.Google ScholarPubMed
Joffe, BI and Kornakova, EE (1998) Notentera ivanovi Joffe et al., 1997: A contribution to the question of phylogenetic relationships between ‘turbellarians’ and the parasitic Platyhelminthes (Neodermata). Hyrdobiologia 383(1), 245250.CrossRefGoogle Scholar
Joffe, BI, Selivanova, RV and Kornakova, EE (1997) Notentera ivanovi n. gen., n. sp. (Turbellaria, Platyhelminthes), a new parasitic turbellarian. Parazitologiya 31(1), 126131.Google Scholar
Jondelius, U, Raikova, OI and Martinez, P (2019) Xenacoelomorpha, a key group to understand bilaterian evolution: morphological and molecular perspectives. pp. 287315 In Pontarotti, P (Ed.) Evolution, origin of life, concepts and methods. Cham, Springer.Google Scholar
Kashitani, M, Okabe, T, Oyama, H, Noguchi, K, Yamazaki, H, Suo, R, Sugita, H and Itoi, S (2020) Taxonomic distribution of tetrodotoxin in acotylean flatworms (Polycladida: Platyhelminthes). Marine Biotechnology 22(6), 805811.CrossRefGoogle Scholar
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious Basic: an integrated and extendable desk-top software platform for the organization and analysis of sequence data. Bioinformatics 28(12), 16471649.CrossRefGoogle Scholar
Klimpel, S, Kuhn, T, Münster, J, Dörge, DD, Klapper, R and Kochmann, J (2019) Parasites of marine fish and cephalopods. 169 pp. Cham, Springer.CrossRefGoogle Scholar
Kornakova, EE and Joffe, BI (1999) A new variant of the neodermatan-type spermiogenesis in a parasitic ‘turbellarian’, Notentera ivanovi (Platyhelminthes) and the origin of the Neodermata. Acta Zoologica 80(2), 135152.CrossRefGoogle Scholar
Kröger, B, Vinther, J and Fuchs, D (2011) Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules: extant cephalopods are younger than previously realised and were under major selection to become agile, shell-less predators. Bioessays 33(8), 602613.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7), 18701874.CrossRefGoogle ScholarPubMed
Kuris, AM, Torchin, ME and Lafferty, KD (2002) Fecampia erythrocephala rediscovered: prevalence and distribution of a parasitoid of the European shore crab, Carcinus maenas. Journal of the Marine Biological Association of the United Kingdom 82(6), 955960.CrossRefGoogle Scholar
Larsson, K, Ahmadzadeh, A and Jondelius, U (2008) DNA taxonomy of Swedish Catenulida (Platyhelminthes) and a phylogenetic framework for catenulid classification. Organisms Diversity & Evolution 8(5), 399412.CrossRefGoogle Scholar
Laumer, CE and Giribet, G (2014) Inclusive taxon sampling suggests a single, stepwise origin of ectolecithality in Platyhelminthes. Biological Journal of the Linnean Society 111(3), 570588.CrossRefGoogle Scholar
Laumer, CE, Hejnol, A and Giribet, G (2015) Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation. eLife 49(1), e05503.CrossRefGoogle Scholar
Lockyer, AE, Olson, PD and Littlewood, DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society 78(2), 155171.CrossRefGoogle Scholar
Noury-Sraïri, N, Justine, JL and Euzet, L (1990) Ultrastructure of the tegument and subepithelial glands of Urastoma cyprinae (Prolecithophora), a turbellarian parasite of molluscs. Annales des Sciences Naturelles, Zoologie et Biologie Animale 11(1), 5371.Google Scholar
Petrov, AF, Kuznetsova, EN, Gordeev, II, et al. (2015) On the Russian scientific observation on fishing of Dissostichus spp. in the CCAMLR area in the season 2014/2015. Trudy VNIRO 155(1), 160165.Google Scholar
Raikova, OI, Kotikova, EA and Frolova, TA (2017) Nervous system and musculature of the parasitic turbellarian Notentera ivanovi (Plathelminthes, Fecampiida). Doklady Biological Sciences 475(1), 169171.CrossRefGoogle Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901–904.CrossRefGoogle ScholarPubMed
Rawlinson, KA, Gillis, JA, Billings, RE and Borneman, EH (2011) Taxonomy and life history of the Acropora-eating flatworm Amakusaplana acroporae nov. sp. (Polycladida: Prosthiostomidae). Coral Reef 30(3), 693705.CrossRefGoogle Scholar
Robledo, JA, Caceres-Martinez, J, Sluys, R and Figueras Huerta, A (1994) The parasitic turbellarian Urastoma cyprinae (Platyhelminthes: Urastomidae) from blue mussel Mytilus galloprovincialis in Spain: occurrence and pathology. Diseases of Aquatic Organisms 18(1), 203210.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12), 15721574.CrossRefGoogle ScholarPubMed
Roumbedakis, K, Drábková, M, Tyml, T and Di Cristo, C (2018) A perspective around cephalopods and their parasites, and suggestions on how to increase knowledge in the field. Frontiers in Physics 9(1), 1573.CrossRefGoogle ScholarPubMed
Scarpa, F, Cossu, P, Delogu, V, Lai, T, Sanna, D, Leasi, F, Norenburg, JL, Curini-Galletti, M and Casu, M (2017) Molecular support for morphology-based family-rank taxa: the contrasting cases of two families of Proseriata (Platyhelminthes). Zoologica Scripta 46(6), 753766.CrossRefGoogle Scholar
Scarpa, F, Sanna, D, Cossu, P, Lai, T, Casu, M and Curini-Galletti, M (2019) How to achieve internal fertilization without a vagina: the study case of the genus Archilina Ax, 1959 (Platyhelminthes, Proseriata) from Canary Islands. Marine Biodiversity 49(3), 20572073.CrossRefGoogle Scholar
Schärer, L, Littlewood, DTJ, Waeschenbach, A, Yoshida, W and Vizoso, DB (2011) Mating behavior and the evolution of sperm design. Proceedings of the National Academy of Sciences of the United States of America 108(4), 14901495.CrossRefGoogle ScholarPubMed
Shinn, GL and Christensen, AM (1985) Kronborgia pugettensis sp.nov. (Neorhabdocoela: Fecampiidae), an endoparasitic turbellarian infesting the shrimp Heptacarpus kincaidi (Rathbun), with notes on its life-history. Parasitology 91(3), 431447.CrossRefGoogle Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9), 13121313.Google ScholarPubMed
Sudo, K, Hirano, YJ and Hirano, YM (2011) Newly discovered parasitic Turbellaria of opisthobranch gastropods. Journal of the Marine Biological Association of the United Kingdom 91(5), 11231133.CrossRefGoogle Scholar
Sukumaran, J and Holder, MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26(12), 15691571.CrossRefGoogle ScholarPubMed
Syromyatnikova, IP (1949) A new turbellarian parasite of fish, Ichthyophaga subcutanea nov. gen., nov. sp. Doklady Akademii Nauk SSSR 68(2), 805808.Google Scholar
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56(4), 564577.CrossRefGoogle ScholarPubMed
Tedesco, P, Bevilacqua, S, Fiorito, G and Terlizzi, A (2020) Global patterns of parasite diversity in cephalopods. Scientific Reports 10(1), 111.CrossRefGoogle ScholarPubMed
Tsunashima, T, Hagiya, M, Yamada, R, Koito, T, Tsuyuki, N, Izawa, S, Kosoba, K, Itoi, S and Sugita, H (2017) A molecular framework for the taxonomy and systematics of Japanese marine turbellarian flatworms (Platyhelminthes, Polycladida). Aquatic Biology 26(1), 159167.CrossRefGoogle Scholar
Tyler, S, Artois, T, Schilling, S, Hooge, M and Bush, LF (Eds) (2006–2022) World list of turbellarian worms: Acoelomorpha, Catenulida, Rhabditophora (formerly class Turbellaria of the phylum Platyhelminthes). Accessed at https://www.marinespecies.org/turbellarians (accessed 25 March 2022).Google Scholar
Waeschenbach, A and Littlewood, DTJ (2017) A molecular framework for the Cestoda. pp. 431451. In Caira, JN and Jensen, K (Eds) Planetary biodiversity inventory (2008–2017): tapeworms from the vertebrate bowels of the earth. Lawrence, Natural History Museum.Google Scholar
Westblad, E (1955) Marine ‘Alloeocoels’(Turbellaria) from North Atlantic and Mediterranean coasts. Arkiv för Zoologi 7(24), 491526.Google Scholar
Westheide, W and Rieger, R (Eds) (1996) Special zoology. Pt. 1: protozoa and invertebrate animals. 909 pp. Stuttgart, Jena, New York, Berlin, Fischer Verlag.Google Scholar
Williams, JB (1988) Further observations on Kronborgia isopodicola, with notes on the systematics of the Fecampiidae (Turbellaria: Rhabdocoela). New Zealand Journal of Zoology 15(2), 211221.CrossRefGoogle Scholar