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Type: Article
Published: 2022-05-19
Page range: 351-387
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Partial redescriptions of three holothurians with “hook papillae” (Apodida: Chiridotidae): Taeniogyrus japonicus (Marenzeller, 1882), T. dendyi (Mortensen, 1925), Scoliorhapis theelii (Heding, 1928)

Wakayama Prefectural Museum of Natural History, Funoo 370-1, Kainan, Wakayama 642-0001, Japan.
Laboratorio de Sistemática y Ecología de Equinodermos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México (UNAM)., Circuito Ext. s/n, Ciudad Universitaria, Mexico City, CP. 04510, México.
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644-0023, Japan. Present address: Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
San'in Kaigan Geopark Museum of the Earth and Sea, 1794-4 Makidani, Iwami, Tottori 681-0001, Japan.
Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan
Marine Biological Station, Sado Island Center for Ecological Sustainability, Niigata University, 87 Tassha, Sado, Niigata 952-2135, Japan.
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644-0023, Japan.
Department of Applied Chemistry and Biochemistry, National Institute of Technology, Wakayama College, 77 Noshima, Nada-cho, Gobo, Wakayama 644-0023, Japan. The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
Echinodermata sea cucumber sigmoid-hooks morphological characters molecular taxonomy Tottori Niigata Sado Island

Abstract

New specimens of Taeniogyrus japonicus (Marenzeller) were collected from Iwami coast and Sado island of the Sea of Japan. According to detailed observations of external and internal organs, we transferred T. japonicus, T. dendyi (Mortensen), and Scoliorhapis theelii (Heding) to the newly revived genus Scoliodota, with a large retractor organ and hook papillae as major diagnostic characters. We also concluded that Scoliorhapis dianthus Solis-marin et al. is a synonym of T. japonicus. Our molecular phylogeny and genetic distance analysis showed that specimens from Iwami and specimens from Sado of T. japonicus form a monophyletic clade, indicating that they are most likely the same species despite their morphological variation. The phylogenetic analysis also indicated that T. japonicus forms a sister group relationship with Taeniogyrus verruculosus Yamana & Tanaka and Scoliorhapis sesokoensis Yamana & Tanaka, suggesting that Taeniogyrus is not monophyletic. Taken together, these results brought new insights to sea cucumber diversity in Japanese waters.

 

References

  1. Becher, S. (1909) Die systematische stellung des Rhabdomolgus novaezealandae. Archives de Zoologie Experimentale et Generale, 5 (1), Notes et Revue 2 (VI), 33–44.
    Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular biology and evolution, 17 (4), 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
    Cherbonnier, G. (1952) Contributions a la connaissance des Holothuries de l'Afrique du Sud. Transactions of the Royal Society of South Africa, 33(4), 469–508. https://doi.org/10.1080/00359195109519895
    Clark, H.L. (1908) The apodous holothurians. Smithsonian Contributions to Knowledge, 35, 1–231.
    Clark, H.L. (1921) The Echinodermata fauna of Torres Strait: its composition and its origin. Carnegie Institution of Washington Publication, 214, 1–233. https://doi.org/10.5962/bhl.title.14613
    Clark, H.L. (1946) Holothurioidea. In: Clark, H.L., The Echinoderm fauna of Australia: its composition and its origin. Carnegie Institution of Washington Publication, 566, 383–461.
    Colgan, D.J., McLauchlan, A., Wilson, G.D.F., Livingston, S.P., Edgecombe, G.D., Macaranas, J., Cassis, G. & Gray, M.R. (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Australian Journal of Zoology, 46 (5), 419–437. https://doi.org/10.1071/ZO98048
    Dawbin, W.H. (1950) A Guide to the Holothurians of New Zealand. Tuatara, 3 (1), 33–41.
    Dendy, A. (1909) On a small collections of Holothurians from the Auckland Islands. In: Chilton, C. (Ed.), The Subantarctic Islands of New Zealand. Vol. I. John Mackay, Government Printer, Dulau & Co Ltd, London, pp. 146–155.
    D'yakonov, A.M., Baranova, Z.I. & Savel'eva, T.S. (1958) [Note on Holothurioidea of the South Sakhalin and South Kurile Islands area.]. Invest. Far-east Seas U.S.S.R., 5, 358–380.
    Heding, S.G. (1928) Synaptidae. Papers from Dr. Th. Mortensen's Pacific Expedition 1914–1916. No. 66. Videnskabelige Meddeleser fra Dansk naturhistorisk Forening i København, 85, 105–323.
    Heding, S.G. (1931) Über die Synaptiden des Zoologischen Museums zu Hamburg. Zoologische Jahrbücher, Abteilung Systematik, 61, 637–696.
    Hoareau, T.B. & Boissin, E. (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Molecular ecology Resources, 10 (6), 960–967. https://doi.org/10.1111/j.1755-0998.2010.02848.x
    Hurvich, C.M. & Tsai, C.L. (1989) Regression and time series model selection in small samples. Biometrika, 76 (2), 297–307. https://doi.org/10.1093/biomet/76.2.297
    Imaoka, T. (1995) Holothuroidea. In: Nishimura, S. (Ed.), Genshoku Kensaku Nihon Kaigan Doubutsu Zukan [Guide to Seashore Animals of Japan with Color Pictures and Keys]. Vol. II. Hoikusha, Osaka, pp. 553–572. [in Japanese]
    Imaoka, T. (2010) Nagashima No Ibokaginamako [Trochodota japonica (von Marenzeller, 1881) from Nagashima Island]. In: Ecological Society of Japan (Ed.), Kiseki No Umi. [The sea of miracles]. Nanpou Shinsha, Kagoshima, pp. 55–56. [in Japanese]
    Inoue, J. & Kajihara, H. (2012) Redescription of Scoliorhapis lindbergi comb. nov. (Echinodermata: Holothuroidea: Apodida: Chiridotidae), with special reference to the ultrastructure of sigmoid bodies. Species Diversity, 17, 15–20. https://doi.org/10.12782/sd.17.1.015
    Jangoux, M. & De Ridder, C. (1990) Annotated catalogue of recent echinoderm type specimens in the collection of the Naturhistorisches Museum Wien. Annotationes Naturhistorisches Museum Wien, 91B, 205–213.
    Joshua, E.C. (1914) Victoria Holothuroidea, with descriptions of New Species. Proceeding of the Royal societies of science of Victoria, New Series, 27 (Part I), 1–11
    Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics, 20 (4), 1160–1166. https://doi.org/10.1093/bib/bbx108
    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of molecular evolution, 16 (2), 111–120. https://doi.org/10.1007/BF01731581
    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular biology and evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054
    Lampert, K. (1885) Die Seewalzen (Holothurioidea) eine systematische monographie. In: Semper, C., Holothurien. Reisen im Archipel der Philippinen. Teil 2. C.W. Kreidel, Wiesbaden, pp. 1–312.
    Ludwig, H. (1889-1892) Die Seewalzen. In: Bronn, H.G. (Ed.), Klassen und Ordnungen des Thier-Reichs, wissenschaftlich dargestellt in Wort und Bild. Zweiter Band. Dritte Abtheilung: Echinodermen (Stachelhäuter). I. Buch. C.F. Winter’sche Verlagshandlung, Leipzig, vi + 460 pp., XVII pls. [1889: pp. 1–176, pls. I–VIII; 1890b: pp. 177–240, pls. IX–XII; 1891b: pp. 241–376, pls. XIII–XVII; 1892a: pp. 377–460, fig. 25]
    Maddison, W.P. & Maddison, D.R. (2018) Mesquite: a modular system for evolutionary analysis. Version 3.5. Available from: http://www.mesquiteproject.org (accessed 27 August 2019)
    Marenzeller, E. (1882 [dated 1881]) Neue Holothurien von Japan and China. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien, 31, 121–140. https://doi.org/10.5962/bhl.part.20315
    Marsh, L.M. & Pawson, D.L. (1993) Echinoderms of Rottnest Island. In: Wells F.E., Walker, D.I., Kirkman, H. & Lethbridge, R. (Eds.), The Marine Flora and Fauna of Rottnest Island, Western Australia, I, pp. 279–304.
    Miller, A.K., Kerr, A.M., Paulay, G., Reich, M., Wilson, N.G., Carvajal, J.I. & Rouse, G.W. (2017) Molecular Phylogeny of Extant Holothuroidea (Echinodermata), Molecular Phylogenetics and Evolution, 111, 110–131. https://doi.org/10.1016/j.ympev.2017.02.014
    Mortensen, T. (1925) Papers from Dr. Th. Mortensen's Pacific Expedition 1914–16. XXIX. Echinoderms of New Zealand and the Auckland-Campbell Islands. III–V. Asteroidea, Holothurioidea and Crinoidea. Videnskabelige Meddeleser fra Dansk naturhistorisk Forening i København, 79, 261–420.
    Moura, R.B., Campos, L. & Esteves, A.M. (2015) Hooked from the deep: a rare new species of Taeniogyrus (Holothuroidea, Chiridotidae) from the continental slope of Brazil, southwestern Atlantic. Zootaxa, 3972 (4), 535–548. https://doi.org/10.11646/zootaxa.3972.4.5
    Murakami, M. (1905) Shasen-rui No Isshu [A species of Sea cucumber]. Dobutsugaku Zasshi [Zoological Magazine], 15, 336–337. [in Japanese]
    Oguro, C. (1961) The fauna of Akkeshi Bay XXVI. Holothuroidea. Publications from the Akkeshi Marine Biological Station, 11, 1–4.
    Ohshima, H. (1913) Synaptiden von Misaki. Dobutsugaku Zasshi, 25, 253–262. https://doi.org/10.4044/joma1889.25.278_253
    Ohshima, H. (1914) The Synaptidae of Japan. Nihon Dobutsugaku Ihou [Annotationes Zoologicae Japonenses], 8, 467–482.
    Ohshima, H. (1915) Report on the holothurians collected by the United States Fisheries Steamer "Albatross" in the Northwestern Pacific during the summer of 1906. Proceedings of the United States National Museum, 48, 213–291. https://doi.org/10.5479/si.00963801.48-2073.213
    Ohshima, H. (1919 [dated 1918]) [Holothuroidea in northwest Pacific. XX]. Dobutsugaku Zasshi [Zoological Magazine], 31, 139–149. [in Japanese]
    O’Loughlin, P.M., Mackenzie, M., VandenSpiegel, D. & Griffiths, H. (2015) New taeniogyrinid species of sea cucumber from the Weddell Sea (Echinodermata: Holothuroidea: Synaptida). Zootaxa, 3995 (1), 271–283.
    https://doi.org/10.11646/zootaxa.3995.1.23
    O’Loughlin, P.M. & VandenSpiegel, D. (2007) New apodid from southern Australia (Echinodermata: Holothuroidea: Apodida). Memoirs of Museum Victoria, 64, 53–70. https://doi.org/10.24199/j.mmv.2007.64.6
    O’Loughlin, P.M. & VandenSpiegel, D. (2010) A revision of Antarctic and Indo-Pacific sea cucumbers (Echinodermata: Holothuroidea: Apodida). Memoirs of Museum Victoria, 67, 61–95. https://doi.org/10.24199/j.mmv.2010.67.06
    Östergren, H. (1898) Das System der Synaptiden. Öfversigt af Kongliga Vetenskaps-Akademiens Förhandlingar, 55, 111–120.
    Ota, Y., Kohtsuka, H. & Yamana, Y. (2021) Echinoderms collected from coastal waters of Tottori Prefecture and adjacent waters, southwestern Sea of Japan. Bulletin of the Hoshizaki Green Foundation, 24, 111–159. [in Japanese with English abstract]
    Parker, T.J. (1881) On a new Holothurian (Chirodota dundinensis n. sp.). Art LXI. Transactions New Zealand Institute, 13, 418.
    Pawson, D.L. (1963) The Holothurian Fauna of Cook Strait, New Zealand. Zoology Publications from Victoria University of Wellington, 36, 1–38.
    Pawson, D.L. (1965) The Distribution of Echinoderms Along the East Coast of New Zealand. Transactions of the Royal Society of New Zealand, Zoology, 24, 245–252.
    Pawson, D.L. (1968) The Echinozoan Fauna of the New Zealand Subantarctic Islands, Macqurie Island and the Chatham Rise. New Zealand Department of Scientific and Industorial Research, 187, Bulletin of the New Zealand Oceanographic Institute, Memoir, No. 42, 1–35.
    Pawson, D.L. (1970) The Marine Fauna of New Zealand: Sea Cucumbers (Echinodermata: Holothuroidea). New Zealand Oceanographic Institute Memoir, No. 52, 1–69.
    Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular ecology, 21 (8), 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
    Rao, G. (1975) On a new interstitial species of Trochodota (Apodida, Holothurioidea) from Andamans, India. Current Science, 44, 508–509.
    Rowe, F.W.E. & Gates, J. (1995) Echinodermata. In: Wells, A. (Ed.), Zoological Catalogue of Australia. Vol. 33. CSIRO, Melbourne, pp. 1–510.
    Rowe, F.W.E., O’Hara T.D. & Bardsley T.M. (2017) Part 2: Echinoderm Diversity, 11: Class Holothuroidea. In: Byrne, M. & O’Hara, T.D. (Eds.), Australian Echinoderms, Biology, Ecology and Evolution. CSIRO, Melbourne, pp. 447–490.
    Salvini-Plawen, L.V. (1972) Zur Taxonomie und Ökologie mediterraner Holothuroidea-Apoda. Helgoländer Wissenschaftliche Meeresuntersuchungen, 23, 459–466. https://doi.org/10.1007/BF01625295
    Schwarz, G. (1978) Estimating the dimension of a model. The annals of statistics, 6 (2), 461–464. https://doi.org/10.1214/aos/1176344136
    Semon, R. (1887) Beiträge zur Naturgeschichte der Synaptiden des Mittelmeers. Mittheilungen aus der Zoologischen Station zu Neapel, Bd. VII, 272–300.
    Semper, C. (1867–1868) Holothurien. Reisen im Archipel der Philippinen, Teil 2, Wissenschaftliche Resultate. C.W. Kreidel, Wiesbaden, 288 pp. https://doi.org/10.5962/bhl.title.11687
    Silvestro, D. & Michalak, I. (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution, 12 (4), 335–337. https://doi.org/10.1007/s13127-011-0056-0
    Smirnov, A.V. (1989) A new species of holothurians Trochodota inexspectata (Synaptida, Chiridotidae) from the Simushir Island (Kuril Islands). Zoologicheskii Zhurnal, 68, 156–160.
    Smirnov, A.V. (1997) New apodid holothurians (Holothurioidea, Apodida) from the New Caledonian continental slope collected during “BIOGEOCAL” expedition 1987. Zoosystema, 19, 15–26.
    Smirnov, A.V. (1998) On the classification of the apodid holothurians. In: Mooi, R. & Telford, M. (Eds.), Echinoderms: San Francisco. Balkema, Rotterdam, pp. 517–522.
    Smirnov, A.V., Panina, E.G., Sanamyan, N.P. & Sanamyan, K.E. (2017) Scoliorhapis stepanovi—new species of sea cucumber from the North-West Pacific (Holothuroidea: Synaptida: Chiridotidae: Taeniogyrinae) and some remarks on the genus Scoliorhapis. Zootaxa, 1337 (4), 563–572. https://doi.org/10.11646/zootaxa.4337.4.7
    Solis-Marin, F.A., Komatsu, M., Soliman, T., Uchida, K., Shimotani, T. & Nozaki, M. (2014) Scoliorhapis dianthus, a new species of sea cucumber (Apodida: Chiridotidae) from the Sea of Japan. Proceedings of the Biological Society of Washington, 127, 323–327. https://doi.org/10.2988/0006-324X-127.2.323
    Studer, T. (1876) Echinodermen aus dem antarktischen Meere und zwei neue Seeigel von den Papua-Inseln, gesammelt auf der Reise S.M.S. Gazelle um die Erde. Monatsbericht der königlich pressischen Akademie der Wissenschaften zu Berlin, 1876, 452–465.
    Théel, H. (1886) Report on the Holothurioidea dredged by H.M.S. Challenger during the years 1873–76. Report of the Scientific Results of the Exploring Voyage of H.M.S. Challenger during the Years 1873–76. Zoology, 39, 1–290.
    Utinomi, H. (1956) Holothuroidea. In: Utinomi, H., Colored Illustrations of Seashore Animals of Japan. Hoikusha, Osaka, pp. 120–122. [in Japanese]
    Utinomi, H. (1965) Holothuroidea. In: Okada, Y., Uchida, S. & Uchida, T. (Eds.), Shin Nihon Doubutsu Zukan. [New Illustrated Encyclopedia of the Fauna of Japan]. Vol. III. Hokuryukan, Tokyo, pp. 82–99. [in Japanese]
    WoRMS (2021) Taeniogyrus Semper, 1867. Available from: https://www.marinespecies.org/aphia.php?p=taxdetails&id=174000 (accessed 31 March 2021)
    Yamana, Y. & Tanaka, H. (2017) Two New Species of Taeniogyrus and Scoliorhapis (Echinodermata: Holothuroidea: Apodida: Chiridotidae: Taeniogyrinae) from Wakayama and Okinawa, Japan. Plankton & Benthos Research, 12, 83–94. https://doi.org/10.3800/pbr.12.83
    Yamana, Y., Tanaka, H. & Nakachi, S. (2017) Three new shallow species of Taeniogyrus and Rowedota (Echinodermata: Holothuroidea: Apodida: Chiridotidae: Taeniogyrinae) from southern Japan. Species diversity, 22, 53–68. https://doi.org/10.12782/sd.22_53
    Yamana, Y., Tanaka H., Hirabayashi, I., Dan, I., Hirai, A. & Ogawa, A. (2022) Three New Infaunal Species of Taeniogyrus (Echinodermata: Holothuroidea: Apodida: Chiridotidae: Taeniogyrinae) from Southern Coast of Wakayama, Japan. Species diversity, 27, 139–158. [in press; disclosed in online first: https://www.jstage.jst.go.jp/article/specdiv/27/1/27_SD21-23/_article/-char/ja] https://doi.org/10.12782/specdiv.27.139
    Zhan, A., Hulák, M., Sylvester, F., Huang, X., Adebayo, A.A., Abbott, C.L., Adamowicz, S.J., Heath, D.D., Cristescu, M.E. & MacIsaac, H.J. (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods in Ecology and Evolution, 4 (6), 558–565. https://doi.org/10.1111/2041-210X.12037