At the edge of the sea: the supralittoral nemertean, Acteonemertes orientalis sp. nov. (Nemertea: Eumonostilifera: Plectonemertidae) from Japan
Natsumi Hookabe
A B * , Yuma Fujino C , Naoto Jimi D E and Rei Ueshima A
+ Author Affiliations
- Author Affiliations
A Research Institute for Global Change (RIGC), Japan Agency for Marine–Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa 237-0061, Japan.
B School of Science, the University of Tokyo, Bunkyo, 113-0033, Japan.
C Tsunai-cho 1-10-11, Tsuruga, Fukui, 914-0056, Japan.
D Sugashima Marine Biological Laboratory, Graduate School of Science, Nagoya University, Toba, 517-0004, Mie, Japan.
E Centre for Marine and Coastal Studies, Universiti Sains Malaysia, 11800, Penang, Malaysia.
Invertebrate Systematics 37(6) 444-456 https://doi.org/10.1071/IS22066
Submitted: 8 December 2022 Accepted: 10 May 2023 Published: 16 June 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.
Abstract
Ribbon worms (phylum Nemertea) are found in oceans worldwide; however, only a few inhabit terrestrial, semiterrestrial and freshwater environments. In our study, we describe Acteonemertes orientalis sp. nov., a new species of Plectonemertidae Gibson, 1990 and the first plectonemertid discovered in Japan. The species was found in the supralittoral zone, from which nemerteans have rarely been reported and inhabits areas under rocks, wave-dissipating concrete blocks, and fallen leaves and stocks, along the coast of the Sea of Japan. Multi-locus phylogenetic analyses based on two mitochondrial (16S rRNA and cytochrome c oxidase subunit I) and two nuclear gene markers (18S rRNA and 28S rRNA) revealed that A. orientalis sp. nov. formed a clade with Leptonemertes cf. chalicophora collected from Florida. Although the external and internal morphology of A. orientalis sp. nov. is largely consistent with the generic diagnosis, this species differs in having a large proboscis. Based on the molecular and morphological data, we propose to amend the diagnosis of Acteonemertes by excluding proboscis size.
ZooBank: urn:lsid:zoobank.org:pub:BBBE9549-5DCE-424F-9A39-930F8243C28B
Keywords: anatomy, Nemertea, phylogeny, species description, systematics, taxonomy, terrestrial, terrestrialisation.
References
Andrade, SCS, Strand, M, Schwartz, M, Chen, H, Kajihara, H, von Döhren, J, Sun, S, Junoy, J, Thiel, M, Norenburg, JL, Turbeville, JM, Giribet, G, and Sundberg, P (2012). Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea. Cladistics 28, 141–159.| Disentangling ribbon worm relationships: multi-locus analysis supports traditional classification of the phylum Nemertea.Crossref | GoogleScholarGoogle Scholar |
Chernyshev, AV, and Polyakova, NE (2019). Nemerteans from the deep-sea expedition KuramBio II with descriptions of three new hoplonemerteans from the Kuril-Kamchatka Trench. Progress in Oceanography 178, 102148.
| Nemerteans from the deep-sea expedition KuramBio II with descriptions of three new hoplonemerteans from the Kuril-Kamchatka Trench.Crossref | GoogleScholarGoogle Scholar |
Durham, MJ (1947). Occurrence of the land nemertine, Geonemertes dendyi Dakin in Wirral, Cheshire. North Western Naturalist 22, 182–183.
Gerlach, J (1998). The behaviour and captive maintenance of the terrestrial nemertine (Geonemertes pelaensis). Journal of Zoology 246, 233–237.
| The behaviour and captive maintenance of the terrestrial nemertine (Geonemertes pelaensis).Crossref | GoogleScholarGoogle Scholar |
Gibson R (1972) ‘Nemerteans.’ (Hutchinson and Co. Ltd: London, UK)
Gibson R (1990) The macrobenthic nemertean fauna of Hong Kong. In ‘Proceedings of the Second International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China. Vol. 1.’ (Ed. BS Morton) pp. 33–212. (Hong Kong University Press: Hong Kong)
Gibson R (1994) ‘Nemerteans.’ (Field Studies Council: Shrewsbury, UK)
Habe, T (1961). Descriptions of fifteen new species of Japanese shells. Venus 21, 416–431.
Hao, Y, Kajihara, H, Chernyshev, AV, Okazaki, RK, and Sun, SC (2015). DNA taxonomy of Paranemertes (Nemertea: Hoplonemertea) with spirally fluted stylets. Zoological Science 32, 571–578.
| DNA taxonomy of Paranemertes (Nemertea: Hoplonemertea) with spirally fluted stylets.Crossref | GoogleScholarGoogle Scholar |
Hickman, VV (1963). The occurrence in Tasmania of the land nemertine, Geonemertes australiensis Dendy, with some account of its distribution, habits, variations and development. Papers and Proceedings of the Royal Society of Tasmania 97, 63–75.
Hookabe, N, Tsuchida, S, Fujiwara, Y, and Kajihara, H (2020). A new species of bathyal nemertean, Proamphiporus kaimeiae sp. nov., off Tohoku, Japan, and molecular systematics of the genus (Nemertea: Monostilifera). Species Diversity 25, 183–188.
| A new species of bathyal nemertean, Proamphiporus kaimeiae sp. nov., off Tohoku, Japan, and molecular systematics of the genus (Nemertea: Monostilifera).Crossref | GoogleScholarGoogle Scholar |
Hookabe, N, Kohtsuka, H, and Kajihara, H (2021). A histology-free description of Tetrastemma cupido sp. nov. (Nemertea: Eumonostilfera) from Sagami Bay, Japan. Marine Biology Research 17, 467–474.
| A histology-free description of Tetrastemma cupido sp. nov. (Nemertea: Eumonostilfera) from Sagami Bay, Japan.Crossref | GoogleScholarGoogle Scholar |
Hookabe, N, Kajihara, H, Chernyshev, AV, Jimi, N, Hasegawa, N, Kohtsuka, H, Okanishi, M, Tani, K, Fujiwara, Y, Tsuchida, S, and Ueshima, R (2022). Molecular phylogeny of the genus Nipponnemertes (Nemertea: Monostilifera: Cratenemertidae) and descriptions of 10 new species, with notes on small body size in a newly discovered clade. Frontiers in Marine Science 9, 906383.
| Molecular phylogeny of the genus Nipponnemertes (Nemertea: Monostilifera: Cratenemertidae) and descriptions of 10 new species, with notes on small body size in a newly discovered clade.Crossref | GoogleScholarGoogle Scholar |
Kajihara, H (2021). Higher classification of the Monostilifera (Nemertea: Hoplonemertea). Zootaxa 4920, 151–199.
| Higher classification of the Monostilifera (Nemertea: Hoplonemertea).Crossref | GoogleScholarGoogle Scholar |
Kajihara, H, Nishi, E, Kawabata, M, Kohtsuka, H, and Uyeno, D (2015). Records of the poorly known ribbon worm Nipponnemertes ogumai (Nemertea: Monostilifera) and its phylogenetic position. Marine Biodiversity 45, 175–182.
| Records of the poorly known ribbon worm Nipponnemertes ogumai (Nemertea: Monostilifera) and its phylogenetic position.Crossref | GoogleScholarGoogle Scholar |
Kajihara, H, Tamura, K, and Tomioka, S (2018). Histology-free descriptions for seven species of interstitial ribbon worms in the genus Ototyphlonemertes (Nemertea: Monostilifera) from Vietnam. Species Diversity 23, 13–37.
| Histology-free descriptions for seven species of interstitial ribbon worms in the genus Ototyphlonemertes (Nemertea: Monostilifera) from Vietnam.Crossref | GoogleScholarGoogle Scholar |
Kumar, S, Stecher, G, and Tamura, K (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar |
Kvist, S, Laumer, CE, Junoy, J, and Giribet, G (2014). New insights into the phylogeny, systematics and DNA barcoding of Nemertea. Invertebrate Systematics 28, 287–308.
| New insights into the phylogeny, systematics and DNA barcoding of Nemertea.Crossref | GoogleScholarGoogle Scholar |
Kvist, S, Chernyshev, AV, and Giribet, G (2015). Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia. Hydrobiologia 760, 105–119.
| Phylogeny of Nemertea with special interest in the placement of diversity from Far East Russia and northeast Asia.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T, and Calcott, B (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Maslakova, SA, and Norenburg, JL (2008). Revision of the smiling worms, genera Prosadenoporus Bürger, 1890 and Pantinonemertes Moore and Gibson, 1981 and description of a new species Prosadenoporus floridensis sp. nov. (Prosorhochmidae; Hoplonemertea; Nemertea) from Florida and Belize. Journal of Natural History 42, 1689–1727.
| Revision of the smiling worms, genera Prosadenoporus Bürger, 1890 and Pantinonemertes Moore and Gibson, 1981 and description of a new species Prosadenoporus floridensis sp. nov. (Prosorhochmidae; Hoplonemertea; Nemertea) from Florida and Belize.Crossref | GoogleScholarGoogle Scholar |
Mateos, E, and Giribet, G (2008). Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass. Zoologica Scripta 37, 235–243.
| Exploring the molecular diversity of terrestrial nemerteans (Hoplonemertea, Monostilifera, Acteonemertidae) in a continental landmass.Crossref | GoogleScholarGoogle Scholar |
McDermott, JJ, and Roe, P (1985). Food, feeding behavior and feeding ecology of nemerteans. American Zoologist 25, 113–125.
| Food, feeding behavior and feeding ecology of nemerteans.Crossref | GoogleScholarGoogle Scholar |
Moore, J (1973). Land nemertines of New Zealand. Zoological Journal of the Linnean Society 52, 293–313.
| Land nemertines of New Zealand.Crossref | GoogleScholarGoogle Scholar |
Moore, J, and Gibson, R (1981). The Geonemertes problem (Nemertea). Journal of Zoology 194, 175–201.
| The Geonemertes problem (Nemertea).Crossref | GoogleScholarGoogle Scholar |
Moore, J, and Gibson, R (1988). Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa. Journal of Zoology 216, 1–20.
| Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa.Crossref | GoogleScholarGoogle Scholar |
Pantin, CFA (1961a). Geonemertes: a study in island life. Proceedings of the Linnean Society of London 172, 137–152.
| Geonemertes: a study in island life.Crossref | GoogleScholarGoogle Scholar |
Pantin, CFA (1961b). Acteonemertes bathamae, gen. et sp. nov. An upper littoral nemertine from Portobello, New Zealand. Proceedings of the Linnean Society of London 172, 153–156.
| Acteonemertes bathamae, gen. et sp. nov. An upper littoral nemertine from Portobello, New Zealand.Crossref | GoogleScholarGoogle Scholar |
Sagorny, C, Wesseler, C, Krämer, D, and von Döhren, J (2019). Assessing the diversity and distribution of Cephalothrix species (Nemertea: Palaeonemertea) in European waters by comparing different species delimitation methods. Journal of Zoological Systematics and Evolutionary Research 57, 497–519.
| Assessing the diversity and distribution of Cephalothrix species (Nemertea: Palaeonemertea) in European waters by comparing different species delimitation methods.Crossref | GoogleScholarGoogle Scholar |
Shinobe, S, Uchida, S, Mori, H, Okochi, I, and Chiba, S (2017). Declining soil crustacea in a world heritage site caused by land nemertean. Scientific Reports 7, 12400.
| Declining soil crustacea in a world heritage site caused by land nemertean.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
| RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar |
Strand, M, and Sundberg, P (2005). Genus Tetrastemma Ehrenberg, 1831 (phylum Nemertea)—a natural group? Phylogenetic relationships inferred from partial 18S rRNA sequences. Molecular Phylogenetics and Evolution 37, 144–152.
| Genus Tetrastemma Ehrenberg, 1831 (phylum Nemertea)—a natural group? Phylogenetic relationships inferred from partial 18S rRNA sequences.Crossref | GoogleScholarGoogle Scholar |
Sundberg, P (1989a). Phylogeny and cladistic classification of the paramonostiliferous family Plectonemertidae (phylum Nemertea). Cladistics 5, 87–100.
| Phylogeny and cladistic classification of the paramonostiliferous family Plectonemertidae (phylum Nemertea).Crossref | GoogleScholarGoogle Scholar |
Sundberg, P (1989b). Classification of the family Plectonemertidae (Nemertea): a phenetic comparison. Zoological journal of the Linnean Society 97, 57–68.
| Classification of the family Plectonemertidae (Nemertea): a phenetic comparison.Crossref | GoogleScholarGoogle Scholar |
Sundberg, P, Kvist, S, and Strand, M (2016). Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea. PLoS One 11, e0155541.
| Evaluating the utility of single-locus DNA barcoding for the identification of ribbon worms (phylum Nemertea.Crossref | GoogleScholarGoogle Scholar |
Thiel, M, and Kruse, I (2001). Status of the Nemertea as predators in marine ecosystems. Hydrobiologia 456, 21–32.
| Status of the Nemertea as predators in marine ecosystems.Crossref | GoogleScholarGoogle Scholar |
Waterston, AR, and Quick, HE (1938). XXIV.—Geonemertes dendyi Dakin, a land nemertean, in Wales. Proceedings of the Royal Society of Edinburgh 57, 379–384.
| XXIV.—Geonemertes dendyi Dakin, a land nemertean, in Wales.Crossref | GoogleScholarGoogle Scholar |
